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Nutrient availability and stoichiometry mediate microbial effects on soil carbon sequestration in tropical forests
Abstract and Figures
The persistence of soil organic carbon (SOC) is primarily driven by microbial metabolic activities; however, how microbial effects on SOC sequestration are affected by soil nutrient status remains unclear. Here, we conducted a one-year-long in situ soil incubation experiment using mesh bags (with a mesh size of 38 µm, allowing bacterial colonization and fungal hyphal penetration while preventing root penetration). This experiment involved incubating fertile sugarcane soil and infertile sand across an elevational gradient, characterized by diverse climatic and biotic conditions within a tropical forest. Biomarkers, such as phospholipid fatty acids, carbon-, nitrogen-, and phosphorus-acquiring hydrolases, glomalin-related proteins, and amino sugars, were measured to characterize the production and accumulation of microbial biomass, exo-enzymes, extracellular glycoproteins, and microbial necromass. These measurements aimed to elucidate their respective contribution to the sequestration of SOC. We found that Gram-negative bacteria dominated the microbial community composition in fertile soil, and the higher nutrient availability was related to the production and accumulation of microbial necromass via promoting microbial biomass turnover, thus enhancing the accumulation of SOC in fertile soil. This process was negatively associated with phosphorus availability and carbon- and phosphorus-acquiring enzyme activities in fertile soil. In contrast, the SOC accumulation was positively correlated with nitrogen availability and stoichiometry (including C:N and C:P), as well as moisture content in infertile sand. However, more resources were preferentially allocated to stress-tolerant fungi and Gram-positive bacteria under nutrient deficiency in infertile sand used for microbial biomass maintenance, nutrient acquisition, and environmental adaption which further aggravated the consumption of SOC, resulting in SOC loss after one year of field incubation. Our results suggest that microbial effects on SOC persistence are highly context-dependent and nutrient availability-induced changes in microbial communities and microbial resource-allocation strategies are key processes for understanding and predicting the fate of carbon in tropical forest soils.
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... Experiments were conducted following the procedures from Indorf et al. (2011) and modifications by (Mou et al., 2023). Briefly, freezedried soil samples (0.5 g, <0.25 mm) were hydrolyzed for 6 h using 10 ml of 6 M HCl at 105 • C. It was then cooled to room temperature and filtered. ...
... The lack of consensus can be ascribed to differences in the technical definition of the successional stage, and other ecological factors (e. g., climate, host diversity and fungal traits) that may overwhelm pedogenesis as a primary determinant of mycorrhizal dominance (but see the review by Dickie et al., 2013). Herein, we propose another possibility that the transitioning effect of litter × soil interaction may also cause inconsistent findings if litter leachates confound with soil substrate availability (Marañón-Jiménez et al., 2021;De Marco et al., 2021Mou et al., 2023). ...
Microbial interactions determine ecosystem carbon (C) and nutrient cycling, yet it remains unclear how interguild fungal interactions modulate microbial residue contribution to soil C pools (SOC) during forest succession. Here, we present a region-wide investigation of the relative dominance of saprophytic versus symbiotic fungi in litter and soil compartments, exploring their linkages to soil microbial residue pools and potential drivers along a chronosequence of secondary Chinese pine (Pinus tabulaeformis) forests on the Loess Plateau. Despite minor changes in C and nitrogen (N) stocks in the litter or soil layers across successional stages, we found significantly lower soil phosphorus (P) stocks, higher ratios of soil C: N, soil N: P and soil C: P but lower ratios of litter C: N and litter C: P in old (> 75 years) than young stands (< 30 years). Pine stand development altered the saprotroph: symbiotroph ratios of fungal communities to favor the soil symbiotrophs versus the litter saprotrophs. The dominance of saprotrophs in litter is positively related to microbial necromass contribution to SOC, which is negatively related to the dominance of symbiotrophs in soils. Antagonistic interguild fungal competition in litter and soil layers, in conjunction with increased fungal but decreased bacterial necromass contribution to SOC, jointly contribute to unchanged total necromass contribution to SOC with stand development. The saprotroph: symbiotroph ratios in litter and soil layers are mainly driven by soil P stocks and stand parameters (e.g., stand age and slope), respectively, while substrate stoichiometries primarily regulate microbial necromass accumulation and fungal: bacterial necromass ratios. These results provide novel insights into how microbial interactions at local spatial scales modulate temporal changes in SOC pools, with management implications for mitigating regional land degradation.
The vegan package provides tools for descriptive community ecology. It has most basic functions of diversity analysis, community ordination and dissimilarity analysis. Most of its multivariate tools can be used for other data types as well.
The functions in the vegan package contain tools for diversity analysis, ordination methods and tools for the analysis of dissimilarities. Together with the labdsv package, the vegan package provides most standard tools of descriptive community analysis. Package ade4 provides an alternative comprehensive package, and several other packages complement vegan and provide tools for deeper analysis in specific fields. Package https://CRAN.R-project.org/package=BiodiversityR provides a Graphical User Interface (GUI) for a large subset of vegan functionality.
The vegan package is developed at GitHub (https://github.com/vegandevs/vegan/). GitHub provides up-to-date information and forums for bug reports. Most important changes in vegan documents can be read with news(package="vegan") and vignettes can be browsed with browseVignettes("vegan"). The vignettes include a vegan FAQ, discussion on design decisions, short introduction to ordination and discussion on diversity methods. A tutorial of the package at http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf provides a more thorough introduction to the package. To see the preferable citation of the package, type citation("vegan").
Understanding the effects of changing climate and long-term human activities on soil organic carbon (SOC) and the mediating roles of microorganisms is critical to maintain soil C stability in agricultural ecosystem. Here, we took samples from a long-term soil transplantation experiment, in which large transects of Mollisol soil in a cold temperate region were translocated to warm temperate and mid-subtropical regions to simulate different climate conditions, with a fertilization treatment on top. This study aimed to understand fertilization effect on SOC and the role of soil microorganisms featured after long-term community incubation in warm climates. After 12 years of soil transplantation, fertilization led to less reduction of SOC, in which aromatic C increased and the consumption of O-alkyl C and carbonyl C decreased. Soil live microbes were analyzed using propidium monoazide to remove DNAs from dead cells, and their network modulization explained 60.4% of variations in soil labile C. Single-cell Raman spectroscopy combined with D 2 O isotope labeling indicated a higher metabolic activity of live microbes to use easily degradable C after soil transplantation. Compared with non-fertilization, there was a significant decrease in soil α-and β-glucosidase and delay on microbial growth with fertilization in warmer climate. Moreover, fertilization significantly increased microbial necromass as indicated by amino sugar content, and its contribution to soil resistant C reached 22.3%. This study evidentially highlights the substantial contribution of soil microbial metabolism and necromass to refractory C of SOC with addition of nutrients in the long-term.
Labile C input to the soil can cause the priming effect (PE) that in turn changes the soil organic C (SOC) content. However, little information is available to predict the magnitude of the PE in different soils, especially under concurrent changes in nutrient inputs. We took advantage of a natural gradient in labile C input in the surroundings of wood ant nests in a temperate coniferous forest which arises through the long-term effects of wood ant foraging on the inputs of honeydew to soil. We collected soils from the surface mineral horizon (high-SOC content) (A horizon) and the subsoil mineral horizon (low-SOC content) (B horizon) at 4 m (low labile C input and higher SOC content) and 70 m (high labile C input and lower SOC content) from four nests. In a 6-month laboratory microcosm experiment, we monitored microbial activity and PE as affected by no nutrient addition (control) or fortnightly additions of labile C alone or in combination with N and/or P (C, CN, CP, CNP). Microbial activity and PE after C addition increased more at 70 m than at 4 m in the B horizon, that is, were higher with a lower SOC content. However, microbial activity and PE in the B horizon were not affected by additions of N and/or P with C. In the A horizon, microbial activity and PE were lower after combined CN addition but increased by combined CP addition relative to C addition alone. In conclusion, labile C inputs had a larger effect on decomposition and PE in low-SOC than high-SOC soils, whereas N and P inputs had greater effects in high-SOC soils than in low-SOC soils. This suggests that low-SOC soils such as those subjected to a high long-term labile C input or those from the subsoil mineral horizon might be more susceptible to increase microbial activity in relation to changes in labile C inputs but less susceptible in relation to changes in N and P inputs relative to high-SOC soils.
Understanding controls on the persistence of soil organic matter (SOM) is essential to constrain its role in the carbon cycle and inform climate-carbon cycle model predictions. Emerging concepts regarding the formation and turnover of SOM imply that it is mainly comprised of mineral-stabilized microbial products and residues; however, direct evidence in support of this concept remains limited. Here, we introduce and test a method for the isolation of isoprenoid and branched glycerol dialkyl glycerol tetraethers (GDGTs)-diagnostic membrane lipids of archaea and bacteria , respectively-for subsequent natural abundance radio-carbon analysis. The method is applied to depth profiles from two Swiss pre-Alpine forested soils. We find that the 14 C values of these microbial markers markedly decrease with increasing soil depth, indicating turnover times of millennia in mineral subsoils. The contrasting metabolisms of the GDGT-producing microorganisms indicates it is unlikely that the low 14 C values of these membrane lipids reflect het-erotrophic acquisition of 14 C-depleted carbon. We therefore attribute the 14 C-depleted signatures of GDGTs to their physical protection through association with mineral surfaces. These findings thus provide strong evidence for the presence of stabilized microbial necromass in forested mineral soils.
The soil nitrogen (N) and phosphorus (P) availability often constrains soil carbon (C) pool, and elevated N deposition could further intensify soil P limitation, which may affect soil C cycling in these N-rich and P-poor ecosystems. Soil microbial residues may not only affect soil organic carbon (SOC) pool, but also impact SOC stability through soil aggregation. However, how soil nutrient availability and aggregate fractions affect microbial residues and the microbial residue contribution to SOC is still not well understood. We took advantage of a 10-year field-fertilization experiment to investigate the effects of nutrient additions, soil aggregate fractions, and their interactions on the concentrations of soil microbial residues and their contribution to SOC accumulation in a tropical coastal forest. We found that continuous P addition greatly decreased the concentrations of microbial residues and their contribution to SOC, whereas N addition had no significant effect. The P-stimulated decreases in microbial residues and their contribution to SOC were presumably due to enhanced recycling of microbial residues via increased activity of residue-decomposing enzymes. The interactive effects between soil aggregate fraction and nutrient addition were not significant, suggesting a weak role of physical protection by soil aggregates in mediating microbial responses to altered soil nutrient availability. Our data suggest that the mechanisms driving microbial residue responses to increased N and P availability might be different, and the P-induced decrease of the contribution of microbial residues might be unfavorable for the stability of SOC in N-rich and P-poor tropical forests. Such information is critical for understanding the role of tropical forests in the global carbon cycle.
Background
China’s terrestrial ecosystems have been receiving increasing amounts of reactive nitrogen (N) over recent decades. External N inputs profoundly change microbially mediated soil carbon (C) dynamics, but how elevated N affects the soil organic C that is derived from microbial residues is not fully understood. Here, we evaluated the changes in soil microbial necromass C under N addition at 11 forest, grassland, and cropland sites over China’s terrestrial ecosystems through a meta-analysis based on available data from published articles.
Results
Microbial necromass C accounted for an average of 49.5% of the total soil organic C across the studied sites, with higher values observed in croplands (53.0%) and lower values in forests (38.6%). Microbial necromass C was significantly increased by 9.5% after N addition, regardless of N forms, with greater stimulation observed for fungal (+ 11.2%) than bacterial (+ 4.5%) necromass C. This increase in microbial necromass C under elevated N was greater under longer experimental periods but showed little variation among different N application rates. The stimulation of soil microbial necromass C under elevated N was proportional to the change in soil organic C.
Conclusions
The stimulation of microbial residues after biomass turnover is an important pathway for the observed increase in soil organic C under N deposition across China’s terrestrial ecosystems.
The global soil carbon (C) pool is massive, so relatively small changes in soil organic carbon (SOC) stocks can significantly alter atmospheric C and global climate. The recently proposed concept of the soil microbial carbon pump (MCP) emphasizes the active role of soil microbes in SOC storage by integrating the continual microbial transformation of organic C from labile to persistent anabolic forms. However, the concept has not been evaluated with data. Here, we combined datasets, including microbial necromass biomarker amino sugars and SOC, from two long‐term agricultural field studies conducted by large United States bioenergy research programs. We interrogate the soil MCP concept by investigating the asynchronous responses of microbial necromass and SOC to land‐use change. Microbial necromass appeared to preferentially accumulate in soil and be the dominant contributor to SOC accrual in diversified perennial bioenergy crops. Specifically, ~92% of the additional SOC enhanced by plant diversity was estimated to be microbial necromass C, and >76% of the additional SOC enhanced by land‐use transition from annual to perennial crops was estimated to be microbial necromass. This suggests that the soil MCP was stimulated in diversified perennial agroecosystems. We further delineate and suggest two parameters–soil MCP capacity and efficacy–reflecting the conversion of plant C into microbial necromass and the contribution of microbial necromass to SOC, respectively that should serve as valuable metrics for future studies evaluating SOC storage under alternative management in changing climates.
Soil organic carbon management has the potential to aid climate change mitigation through drawdown of atmospheric carbon dioxide. To be effective, such management must account for processes influencing carbon storage and re-emission at different space and time scales. Achieving this requires a conceptual advance in our understanding to link carbon dynamics from the scales at which processes occur to the scales at which decisions are made. Here, we propose that soil carbon persistence can be understood through the lens of decomposers as a result of functional complexity derived from the interplay between spatial and temporal variation of molecular diversity and composition. For example, co-location alone can determine whether a molecule is decomposed, with rapid changes in moisture leading to transport of organic matter and constraining the fitness of the microbial community, while greater molecular diversity may increase the metabolic demand of, and thus potentially limit, decomposition. This conceptual shift accounts for emergent behaviour of the microbial community and would enable soil carbon changes to be predicted without invoking recalcitrant carbon forms that have not been observed experimentally. Functional complexity as a driver of soil carbon persistence suggests soil management should be based on constant care rather than one-time action to lock away carbon in soils. Dynamic interactions between chemical and biological controls govern the stability of soil organic carbon and drive complex, emergent patterns in soil carbon persistence.
Soil carbon transformation and sequestration have received significant interest in recent years due to a growing need for quantifying its role in mitigating climate change. Even though our understanding of the nature of soil organic matter has recently been substantially revised, fundamental uncertainty remains about the quantitative importance of microbial necromass as part of persistent organic matter. Addressing this uncertainty has been hampered by the absence of quantitative assessments whether microbial matter makes up the majority of the persistent carbon in soil. Direct quantification of microbial necromass in soil is very challenging because of overlapping molecular signature with non‐microbial organic carbon. Here we use a comprehensive analysis of existing biomarker amino sugar data published between 1996‐2018, combined with novel appropriation using ecological systems approach, elemental carbon‐nitrogen stoichiometry, and biomarker scaling, to demonstrate a suit of strategies for quantifying the contribution of microbe‐derived carbon to the topsoil organic carbon reservoir in global temperate agricultural, grassland, and forest ecosystems. We show that microbial necromass can make up more than half of soil organic carbon. Hence, we suggest next‐generation field management requires promoting microbial biomass formation and necromass preservation to maintain healthy soils, ecosystems, and climate. Our analyses have important implications for improving current climate and carbon models, and helping develop management practices and policies. This article is protected by copyright. All rights reserved.
Core Ideas
Plant mucilage and bacterial extracellular polymeric substances (EPS) prevent the breakup of the soil liquid phase.
Formation of continuous structures buffers soil hydraulic properties.
The release of viscous polymeric substances represents a universal strategy.
Plant roots and bacteria are capable of buffering erratic fluctuations of water content in their local soil environment by releasing a diverse, highly polymeric blend of substances (e.g. extracellular polymeric substances [EPS] and mucilage). Although this concept is well accepted, the physical mechanisms by which EPS and mucilage interact with the soil matrix and determine the soil water dynamics remain unclear. High‐resolution X‐ray computed tomography revealed that upon drying in porous media, mucilage (from maize [Zea mays L.] roots) and EPS (from intact biocrusts) form filaments and two‐dimensional interconnected structures spanning across multiple pores. Unlike water, these mucilage and EPS structures connecting soil particles did not break up upon drying, which is explained by the high viscosity and low surface tension of EPS and mucilage. Measurements of water retention and evaporation with soils mixed with seed mucilage show how these one‐ and two‐dimensional pore‐scale structures affect macroscopic hydraulic properties (i.e., they enhance water retention, preserve the continuity of the liquid phase in drying soils, and decrease vapor diffusivity and local drying rates). In conclusion, we propose that the release of viscous polymeric substances and the consequent creation of a network bridging the soil pore space represent a universal strategy of plants and bacteria to engineer their own soil microhydrological niches where stable conditions for life are preserved.
Amino sugars are important indices for the contribution of soil microorganisms to soil organic matter. Consequently, the past decade has seen a great increase in the number of studies measuring amino sugars. However, some uncertainties remain in the interpretation of amino sugar data. The objective of the current opinion paper is to summarize current knowledge on amino sugars in soils, to give some advice for future research objectives, and to make a plea for the correct use of information. The study gives an overview on the origin of muramic acid (MurN), glucosamine (GlcN), galactosamine (GalN), and mannosamine (ManN). Information is also provided on measuring total amino sugars in soil but also on compound-specific δ¹³C and δ¹⁵N determination. Special attention is given to the turnover of microbial cell-wall residues, to the interpretation of the GlcN/GalN ratio, and to the reasons for converting fungal GlcN and MurN to microbial residue C. There is no evidence to suggest that the turnover of fungal residues generally differs from that of bacterial residues. On average, MurN contributes 7% to total amino sugars in soil, GlcN 60%, GalN 30%, and ManN 4%. MurN is highly specific for bacteria, GlcN for fungi if corrected for the contribution of bacterial GlcN, whereas GalN and ManN are unspecific microbial markers.
Crop residue quality and quantity have contrasting effects on soil organic matter (SOM) decomposition, but the mechanisms explaining such priming effect (PE) are still elusive. To reveal the role of residue quality and quantity in SOM priming, we applied two rates (5.4–10.8 g kg−1) of 13C-labeled wheat residues (separately: leaves, stems, roots) to soil and incubated for 120 days. To distinguish PE mechanisms, labeled C was traced in CO2 efflux and in microbial biomass and enzyme activities (involved in C, N, and P cycles) were measured during the incubation period. Regardless of residue type, PE intensity declined with increasing C additions. Roots were least mineralized but caused up to 60% higher PE compared to leaves or stems. During intensive residue mineralization (first 2–3 weeks), the low or negative PE resulted from pool substitution. Thereafter (15–60 days), a large decline in microbial biomass along with increased enzyme activity suggested that microbial necromass served as SOM primer. Finally, incorporation of SOM-derived C into remaining microbial biomass corresponded to increased enzyme activity, which is indicative of SOM cometabolism. Both PE and enzyme activities were primarily correlated with residue-metabolizing soil microorganisms. A unifying model demonstrated that PE was a function of residue mineralization, with thresholds for strong PE increase of up to 20% root, 44% stem, and 51% leaf mineralization. Thus, root mineralization has the lowest threshold for a strong PE increase. Our study emphasizes the role of residue-feeding microorganisms as active players in the PE, which are mediated by quality and quantity of crop residue additions.
Communities of litter saprotrophic and root‐associated fungi are vertically separated within boreal forest soil profiles. It is unclear whether this depth partitioning is maintained exclusively by substrate‐mediated niche partitioning (i.e. distinct fundamental niches), or by competition for space and resources (i.e. distinct realized niches). Improved understanding of the mechanisms driving spatial partitioning of these fungal guilds is critical, as they modulate carbon and nutrient cycling in different ways.
Under field settings, we tested the effects of substrate quality and the local fungal species pool at various depths in determining the potential of saprotrophic and mycorrhizal fungi to colonize and exploit organic matter. Natural substrates of three qualities – fresh or partly decomposed litter or humus – were incubated in the corresponding organic layers of a boreal forest soil profile in a fully factorial design. After one and two growing seasons, fungal community composition in the substrates was determined by 454‐pyrosequencing and decomposition was analyzed.
Fungal community development during the course of the experiment was determined to similar degrees by vertical location of the substrates (24% of explained variation) and by substrate quality (20%), indicating that interference competition is a strong additional driver of the substrate‐dependent depth partitioning of fungal guilds in the system. During the first growing season, litter substrates decomposed slower when colonized by root‐associated communities than when colonized by communities of litter saprotrophs, whereas humus was only slightly decomposed by both fungal guilds. During the second season, certain basidiomycetes from both guilds were particularly efficient in localizing and exploiting their native organic substrates although displaced in the vertical profile. This validates that fungal community composition, rather than microclimatic factors, were responsible for observed depth‐related differences in decomposer activities during the first season.
In conclusion, our results suggest that saprotrophic and root‐associated fungal guilds have overlapping fundamental niches with respect to colonization of substrates of different qualities, and that their substrate‐dependent depth partitioning in soils of ectomycorrhiza‐dominated ecosystems is reinforced by interference competition. Through competitive interactions, mycorrhizal fungi can thus indirectly regulate litter decomposition rates by restraining activities of more efficient litter saprotrophs.
A lay summary is available for this article.
Temperature regulates the rate of biogeochemical cycles. One way it does so is through control of microbial metabolism. Warming effects on metabolism change with time as physiology adjusts to the new temperature. I here propose that such thermal adaptation is observed in soil microbial respiration and growth, as the result of universal evolutionary trade-offs between the structure and function of both enzymes and membranes. I review the basis for these trade-offs and show that they, like substrate depletion, are plausible mechanisms explaining soil respiration responses to warming. I argue that controversies over whether soil microbes adapt to warming stem from disregarding the evolutionary physiology of cellular metabolism, and confusion arising from the term thermal acclimation to represent phenomena at the organism- and ecosystem-levels with different underlying mechanisms. Measurable physiological adjustments of the soil microbial biomass reflect shifts from colder- to warmer-adapted taxa. Hypothesized declines in the growth efficiency of soil microbial biomass under warming are controversial given limited data and a weak theoretical basis. I suggest that energy spilling (aka waste metabolism) is a more plausible mechanism for efficiency declines than the commonly invoked increase in maintenance-energy demands. Energy spilling has many fitness benefits for microbes and its response to climate warming is uncertain. Modeled responses of soil carbon to warming are sensitive to microbial growth efficiency, but declines in efficiency mitigate warming-induced carbon losses in microbial models and exacerbate them in conventional models. Both modeling structures assume that microbes regulate soil carbon turnover, highlighting the need for a third structure where microbes are not regulators. I conclude that microbial physiology must be considered if we are to have confidence in projected feedbacks between soil carbon stocks, atmospheric CO2, and climate change.
Society relies on Earth system models (ESMs) to project future climate and carbon (C) cycle feedbacks. However, the soil C response to climate change is highly uncertain in these models1, 2 and they omit key biogeochemical mechanisms3, 4, 5. Specifically, the traditional approach in ESMs lacks direct microbial control over soil C dynamics6, 7, 8. Thus, we tested a new model that explicitly represents microbial mechanisms of soil C cycling on the global scale. Compared with traditional models, the microbial model simulates soil C pools that more closely match contemporary observations. It also projects a much wider range of soil C responses to climate change over the twenty-first century. Global soils accumulate C if microbial growth efficiency declines with warming in the microbial model. If growth efficiency adapts to warming, the microbial model projects large soil C losses. By comparison, traditional models project modest soil C losses with global warming. Microbes also change the soil response to increased C inputs, as might occur with CO2 or nutrient fertilization. In the microbial model, microbes consume these additional inputs; whereas in traditional models, additional inputs lead to C storage. Our results indicate that ESMs should simulate microbial physiology to more accurately project climate change feedbacks.
Lignins are amongst the most studied bio-macromolecules in natural environments, for their properties as biomarkers and their suggested influence on soil organic carbon dynamics. A large number of methods exists to characterize lignins, but the alkaline CuO oxidation is the most used for determining lignin fate in soils. The CuO oxidation products of lignins yield quantitative information (sum of V, S and C monomers) as well as qualitative information on the degradation of lignins (S/V, C/V, (Ad/Al)V,S...). The CuO-lignin products provide information on lignins but also on the environment and particularly on the present and past vegetation. Data from several studies were compiled in order to evaluate the relations between lignins in soils and various environmental parameters. The results of the multiple correspondence analysis (MCA) performed suggest that the lignin content in soils is directly related to the C and N contents, confirming its contribution to the pool of organic carbon. The lignin distribution appears also related to the climate and to the soil texture, which suggests the impact of these parameters on the lignin degradation and retention in soils, as observed for organic carbon (Burke et al., 1989). The total lignin content generally decreases with the soil depth and with the decreasing size of the granulometric fractions. Hence, the more lignins are degraded, the more they are associated with the finest fractions. In addition, it appears that lignin contents are linked to land-use. Thus, in accordance with the land cover, management type and amount of annual input, the forest soils are described by high contents of VSC, C and N, in contrast with the arable land. Lignins were often considered to greatly participate to the stock of slowly degradable and stable carbon in soils. However, several studies suggest that lignin turnover can be more rapid than that of the bulk soil organic carbon (SOC), suggesting that they are not stabilized in soil. On the other hand, other studies suggest contradictory results, suggesting the retention of a large part of the initial lignin input and its preservation in the organo-mineral fraction (Hofmann et al., 2009; Dümig et al., 2009). This contradiction could be due to the existence of two pools of lignins in soils: one pool of fresh lignin residues with a fast turnover and one of protected lignins with a slow turnover (Lobe et al., 2002; Rasse et al., 2006). However, the mechanisms of protection are not yet clear, and could be related to chemical variation in the structure of the lignins leading a decrease of their degradability (chemical protection) and/or to interactions between a fraction of the lignins with the mineral phase of the soil (physical protection). In conclusion, this review suggests that lignins greatly influence the bulk SOC dynamics, but their fate in soils needs to be elucidated. To this end, the future researches could focus on the relations between the lignin distribution and the environmental parameters, and on the kinetic pools of lignins in soils. Burke I.C., Yonker C.M., Parton W. J., Cole C. V., Schimel D. S., Flach K., 1989. Soil Science Society of America Journal 53, 800-805. Dümig A., Rumpel C., Dignac M.-F., Schad P., Ingrid Kögel-Knabner I., 2008. Organic Geochemistry, Submitted. Lobe I., Du Preez C.C, Amelung A., 2002. European Journal of Soil Science 53, 553-562. Hofmann A., Heim A., Christensen B.T., Miltner A., Gehre M., Schmidt M.W.I., 2009. European Journal of Soil Science, Accepted. Rasse D.P., Dignac M.-F., Bahri H., Rumpel C., Mariotti A., Chenu C., 2006. European Journal of Soil Science 57, 530-538.
The availability of Soil Organic Nitrogen (SON) determines soil fertility and biomass production to a great extent. SON also affects the amounts and turnover rates of the soil organic carbon (SOC) pools. Although there is increasing awareness of the impact of the nitrogen (N) cycle on the carbon (C) cycle, the extent of this interaction and the implications for soil organic matter (SOM) dynamics are still under debate. Therefore, present knowledge about the inter-relationships of the soil cycles of C and N as well as current ideas about SON stabilization are summarized in this paper in order to develop an advanced concept of the role of N on C sequestration. Modeling global C-cycling, it was already recognized that SON and SOC are closely coupled via biomass production and degradation. However, the narrow C/N ratio of mature soil organic matter (SOM) shows further that the impact of SON on the refractory SOM is beyond that of determining the size of the active cycling entities. It affects the quantity of the slow cycling pool and as a major contributor it also determines its chemical composition. Although the chemical nature of SON is still not very well understood, both improved classical wet chemical analyses and modern spectroscopic techniques provide increasing evidence that almost the entire organic N in fire-unaffected soils is bound in peptide-like compounds and to a lesser extent in amino sugars. This clearly points to the conclusion, that such compounds have greater importance for SOM formation than previously assumed. Based on published papers, I suggest that peptides even have a key function in the C-sequestration process. Although the mechanisms involved in their medium and long-term stabilization are far from understood, the immobilization of these biomolecules seems to determine the chemistry and functionality of the slow cycling SOM fraction and even the potential of a soil to act as a C sink. Pyrogenic organic N, which derives mostly from incomplete combustion of plant and litter peptides is another under-rated player in soil organic matter preservation. In fire-prone regions, its formation represents a major N stabilization mechanism, leading to the accumulation of heterocyclic aromatic N, the stability of which is still not elaborated. The concept of peptide-like compounds as a key in SOM-sequestration implies that for an improved evaluation of the potential of soils as C-sinks our research focus as to be directed to a better understanding of their chemistry and of the mechanisms which are responsible for their resistance against biochemical degradation in soils.
A major thrust of terrestrial microbial ecology is focused on understanding when and how the composition of the microbial community affects the functioning of biogeochemical processes at the ecosystem scale (meters-to-kilometers and days-to-years). While research has demonstrated these linkages for physiologically and phylogenetically “narrow” processes such as trace gas emissions and nitrification, there is less conclusive evidence that microbial community composition influences the “broad” processes of decomposition and organic matter (OM) turnover in soil. In this paper, we consider how soil microbial community structure influences C cycling. We consider the phylogenetic level at which microbes form meaningful guilds, based on overall life history strategies, and suggest that these are associated with deep evolutionary divergences, while much of the species-level diversity probably reflects functional redundancy. We then consider under what conditions it is possible for differences among microbes to affect process dynamics, and argue that while microbial community structure may be important in the rate of OM breakdown in the rhizosphere and in detritus, it is likely not important in the mineral soil. In mineral soil, physical access to occluded or sorbed substrates is the rate-limiting process. Microbial community influences on OM turnover in mineral soils are based on how organisms allocate the C they take up – not only do the fates of the molecules differ, but they can affect the soil system differently as well. For example, extracellular enzymes and extracellular polysaccharides can be key controls on soil structure and function. How microbes allocate C may also be particularly important for understanding the long-term fate of C in soil – is it sequestered or not?
Soil salinity (high levels of water-soluble salt) and sodicity (high levels of exchangeable sodium), called collectively salt-affected soils, affect approximately 932 million ha of land globally. Saline and sodic landscapes are subjected to modified hydrologic processes which can impact upon soil chemistry, carbon and nutrient cycling, and organic matter decomposition. The soil organic carbon (SOC) pool is the largest terrestrial carbon pool, with the level of SOC an important measure of a soil’s health. Because the SOC pool is dependent on inputs from vegetation, the effects of salinity and sodicity on plant health adversely impacts upon SOC stocks in salt-affected areas, generally leading to less SOC. Saline and sodic soils are subjected to a number of opposing processes which affect the soil microbial biomass and microbial activity, changing CO2 fluxes and the nature and delivery of nutrients to vegetation. Sodic soils compound SOC loss by increasing dispersion of aggregates, which increases SOC mineralisation, and increasing bulk density which restricts access to substrate for mineralisation. Saline conditions can increase the decomposability of soil organic matter but also restrict access to substrates due to flocculation of aggregates as a result of high concentrations of soluble salts. Saline and sodic soils usually contain carbonates, which complicates the carbon (C) dynamics. This paper reviews soil processes that commonly occur in saline and sodic soils, and their effect on C stocks and fluxes to identify the key issues involved in the decomposition of soil organic matter and soil aggregation processes which need to be addressed to fully understand C dynamics in salt-affected soils.
Soil organic matter is the dominant carbon pool in terrestrial ecosystems, and its management is of increasing policy relevance. Soil microbes are the main drivers of soil organic carbon sequestration, especially through accumulation of their necromass. However, since the direct characterization of microbial necromass in soil is challenging, its composition and formation remain unresolved. Here we provide evidence that microbial death pathways (the distinct processes of microbial dying) in soil affect necromass composition and its subsequent fate. Importantly, the composition of derived microbial necromass does not equal that of microbial biomass. From biomass to necromass, distinct chemical transformations lead to increases in cell wall/cytoplasm ratios while nutrient contents and easily degradable compounds are depleted. The exact changes depend on environmental conditions and the relevance of different microbial death pathways, for example, predation, starvation or anthropogenic stresses. This has far-reaching consequences for mechanisms underpinning biogeochemical processes: (1) the quantity and persistence of microbial necromass is governed by microbial death pathways, not only the initial biomass composition; (2) efficient recycling of nutrients within microbial biomass presents a possible pathway of organic carbon sequestration that minimizes nitrogen losses; (3) human-induced disturbances affect the causes of microbial death and consequently necromass composition. Thus, new research focusing on microbial death pathways holds great potential to improve management strategies for soil organic carbon storage. Not only microbial growth but also death drive the soil microbial carbon pump. Microbial death pathways affect the quantity and composition of microbial necromass and its associated soil organic carbon.
Microorganisms govern soil nutrient cycling. It is therefore critical to understand their responses to human-induced increases in N and P inputs. We investigated microbial community composition, biomass, functional gene abundance, and enzyme activities in response to 10-year N and P addition in a primary tropical montane forest, and we explored the drivers behind these effects. Fungi were more sensitive to nutrient addition than bacteria, and the fungal community shift was mainly driven by P availability. N addition aggravated P limitation, to which microbes responded by increasing the abundance of P cycling functional genes and phosphatase activity. In contrast, P addition alleviated P deficiency, and thus P cycling functional gene abundance and phosphatase activity decreased. The shift of microbial community composition, changes in functional genes involved in P cycling, and phosphatase activity were mainly driven by P addition, which also induced the alteration of soil stoichiometry (C/P and N/P). Eliminating P deficiency through fertilization accelerated C cycling by increasing the activity of C degradation enzymes. The abundances of C and P functional genes were positively correlated, indicating the intensive coupling of C and P cycling in P-limited forest soil. In summary, a long-term fertilization experiment demonstrated that soil microorganisms could adapt to induced environmental changes in soil nutrient stoichiometry, not only through shifts of microbial community composition and functional gene abundances, but also through the regulation of enzyme production. The response of the microbial community to N and P imbalance and effects of the microbial community on soil nutrient cycling should be incorporated into the ecosystem biogeochemical model.
Microbial biomass is increasingly considered to be the main source of organic carbon (C) sequestration in soils. Quantitative information on the contribution of microbial necromass to soil organic carbon (SOC) formation and the factors driving necromass accumulation, decomposition and stabilization during the initial soil formation in biological crusts (biocrusts) is absent. To address this knowledge gap, we investigated the composition of microbial necromass and its contributions to SOC sequestration in a biocrust formation sequence consisting of five stages: bare sand, cyanobacteria stage, cyanobacteria-moss stage, moss-cyanobacteria stage, and moss stage on sandy parent material on the Loess Plateau. The fungal and bacterial necromass C content in soil was analyzed based on amino sugars - the cell wall biomarker. Microbial necromass was an important source of SOC, and was incorporated into the particulate and mineral-associated organic C (MAOC). Because bacteria have smaller and thinner cell wall fragments as well as more proteins than fungi, bacterial necromass mainly contributed to the MAOC pool, while fungal residues remained more in the particulate organic C (POC). MAOC pool was saturated fast with the increase of microbial necromass, and POC more rapid accumulation than MAOC suggests that the clay content was the limiting factor for stable C accumulation in this sandy soil. The necromass exceeding the MAOC stabilization level was stored in the labile POC pool (especially necromass from fungi). Activities of four enzymes (i.e., β-1,4-glucosidase, β-1,4-N-acetyl-glucosaminidase, leucine aminopeptidase, and alkaline phosphatase) increasing with fungal and bacterial necromass suggest that the raised activity of living microorganisms accelerated the turnover and formation of necromass. Microbial N limitation raised the production of N acquisition enzymes (e.g., β-1,4-N-acetyl-glucosaminidase and leucine aminopeptidase) to break down necromass compounds, leading to further increase of the nutrient pool in soil solution. The decrease of microbial N limitation along the biocrusts formation chronosequence is an important factor for the necromass accumulation during initial soil development. High microbial N demands and insufficient clay protection lead to fast necromass reutilization by microorganisms and thus, result in a low necromass accumulation coefficient, that is, the ratio of microbial necromass to living microbial biomass (on average, 9.6). Consequently, microbial necromass contribution to SOC during initial soil formation by biocrust is lower (12–25%) than in fully developed soils (33%–60%, literature data). Nitrogen (N) limitation of microorganisms and an increased ratio between N-acquiring enzyme activities and microbial N, as well as limited clay protection, resulted in a low contribution of microbial necromass to SOC by initial formation of biocrust-covered sandy soil. Summarizing, soil development leads not only to SOC accumulation, but also to increased contribution of microbial necromass to SOC, whereas the plant litter contribution decreases.
High nitrogen (N) and phosphorus (P) availability has significant influence on microbial-driven soil carbon (C) sequestration. Microbial residues are a significant contributor of soil stable C pool, their distribution among aggregate fractions determines long-term soil C stability. However, very little is known about the interactive effects of N and P fertilization on soil microbes, especially their residues, at aggregate scale in plantation ecosystems. Since 2012, a field-manipulated experiment with N (200 kg N ha − 1 year − 1) and/or P fertilization (50 kg P ha − 1 year − 1) has been conducted to examine their interactive effects on microbial community and residues in bulk soil and three soil aggregate fractions: large macroaggregates (>2 mm, LMA), small macroaggregates (0.25-2 mm, SMA), and microaggregates (<0.25 mm, MA) in a subtropical Chinese fir (Cunninghamia lanceolata) plantation. Results showed that N and P fertilization, either individually or in combination, decreased microbial biomass of bulk soils to a similar extent (by up to 37.0%). This reduction was due to the decreased bacterial biomass in SMA and MA and fungi in LMA. By contrast, adding N and P fertilizer together (NP) significantly stimulated fungal residues in SMA and further redistributed microbial residues from LMA to SMA, although single fertilization had no effects on microbial residues or their distribution. Changes in root biomass moderated the direct effects of fertilization on aggregate-associated microbial groups and the indirect effects of NP fertilization on microbial residue distribution. Together, our results provide new insights into the microbial mechanisms through which multiple fertilization control soil C persistence in subtropical plantation. These findings highlight that separating bulk soil into distinct aggregate fractions and considering the interactive effect of N and P fertilization are needed to predict the soil C dynamics under fertilization.
Despite the recognized importance of the contribution of microbial necromass to soil organic carbon (SOC) sequestration, at a global scale, there has been no quantification for cropland, grassland, and forest ecosystems. To address this knowledge gap, the contents of fungal and bacterial necromass were estimated based on glucosamine and muramic acid contents in cropland (986 samples), grassland (278 samples), and forest (452 samples) soils. On an average, microbial necromass C contributed 51%, 47%, and 35% to the SOC in cropland, grassland, and forest soils, respectively, in the first 20 cm of topsoil. The contribution of microbial necromass to SOC increased with soil depth in grasslands (from 47% to 54%) and forests (from 34% to 44%), while it decreased in croplands (from 51% to 24%). The microbial necromass accumulation coefficient (the ratio between necromass and living microbial biomass C) was higher in soil from croplands (41) and grasslands (33) than in forest (20) soils. These results suggest that the turnover of living microbial biomass is faster in grassland and cropland soils than in forest soils, where the latter contains more partially decomposed plant residues. Fungal necromass C (>65% of total necromass) had consistently higher contributions to SOC than bacterial necromass C (32-36%) in all soils due to i) a larger living fungal biomass than bacterial biomass, and ii) fungal cell compounds being decomposed slowly and, thus able to persist longer in soil. The ratio of fungal:bacterial necromass C increased from 2.4 to 2.9 in the order of croplands < grasslands < forests, because fungi are the principal decomposers of complex substrates dominant in grassland and, especially, in forest soils. The ratios of bacterial: microbial necromass and bacterial:fungal necromass in cropland soils are larger than those in grassland and forest soils. This result indicates that the relative contribution of fungal necromass to total microbial necromass is lowest in cropland among the three land uses. Moreover, fungal and bacterial necromass increased with the total living microbial C and N contents. Lower temperatures and soil pH (e.g., in temperate and boreal ecosystems) stimulate fungal and bacterial necromass accumulation. These findings highlight the fact that shifts in the bacterial:fungal necromass ratio and the microbial necromass contribution to SOC are ecosystem-specific and depend on climate. In conclusion, microbial necromass contributes to approximately half of the SOC in cropland and grassland soils, and only 35% in forest soils; whereas, two-thirds of microbial necromass are of fungal origin.
Despite the recognized importance of the contribution of microbial necromass to soil organic carbon (SOC) sequestration, at a global scale, there has been no quantification for cropland, grassland, and forest ecosystems. To address this knowledge gap, the contents of fungal and bacterial necromass were estimated based on glucosamine and muramic acid contents in cropland (986 samples), grassland (278 samples), and forest (452 samples) soils. On an average, microbial necromass C contributed 51%, 47%, and 35% to the SOC in cropland, grassland, and forest soils, respectively, in the first 20 cm of topsoil. The contribution of microbial necromass to SOC increased with soil depth in grasslands (from 47% to 54%) and forests (from 34% to 44%), while it decreased in croplands (from 51% to 24%). The microbial necromass accumulation coefficient (the ratio between necromass and living microbial biomass C) was higher in soil from croplands (41) and grasslands (33) than in forest (20) soils. These results suggest that the turnover of living microbial biomass is faster in grassland and cropland soils than in forest soils, where the latter contains more partially decomposed plant residues. Fungal necromass C (>65% of total necromass) had consistently higher contributions to SOC than bacterial necromass C (32–36%) in all soils due to i) a larger living fungal biomass than bacterial biomass, and ii) fungal cell compounds being decomposed slowly and, thus able to persist longer in soil. The ratio of fungal:bacterial necromass C increased from 2.4 to 2.9 in the order of croplands < grasslands < forests, because fungi are the principal decomposers of complex substrates dominant in grassland and, especially, in forest soils. The ratios of bacterial:microbial necromass and bacterial:fungal necromass in cropland soils are larger than those in grassland and forest soils. This result indicates that the relative contribution of fungal necromass to total microbial necromass is lowest in cropland among the three land uses. Moreover, fungal and bacterial necromass increased with the total living microbial C and N contents. Lower temperatures and soil pH (e.g., in temperate and boreal ecosystems) stimulate fungal and bacterial necromass accumulation. These findings highlight the fact that shifts in the bacterial:fungal necromass ratio and the microbial necromass contribution to SOC are ecosystem-specific and depend on climate. In conclusion, microbial necromass contributes to approximately half of the SOC in cropland and grassland soils, and only 35% in forest soils; whereas, two-thirds of microbial necromass are of fungal origin.
Microbial residues may make a more significant contribution to soil organic carbon (SOC) than traditionally believed. However, little is known about the accumulation characteristics of fungal and bacterial residues and their contribution to SOC in salt-affected soils. We investigated changes in fungal and bacterial residues using amino sugar biomarkers along a salinity gradient in coastal salt-affected soils. As salinity increased, the content of fungal residue decreased from 337.57 to 111.60 mg kg⁻¹, while the bacterial counterpart increased from 62.53 to 142.37 mg kg⁻¹. The contribution of microbial residues to SOC was salinity-dependent. There was an increase for microbial residue contribution to SOC and a shift from fungal to bacterial residue dominated contribution to SOC with increasing salinity. Hence, salinization had a significant impact on microbial-mediated SOC accumulation.
Microbial necromass carbon (MNC) is key to soil organic carbon (SOC) storage. However, mechanisms regulating MNC accumulation on large scales are poorly understood. Here we provide the first batch of regional-scale MNC data based on amino sugars for the Qinghai-Tibet Plateau alpine grasslands. We show that Qinghai-Tibet grasslands have similar microbial biomass carbon (MBC) but lower MNC concentrations in SOC than Mongolian and other grasslands. The low contribution of MNC to SOC is mainly attributed to high aridity and low net primary productivity of the Qinghai-Tibet grasslands. Our findings highlight climatic and plant influences on MNC accumulation at regional scales.
Microbial residues play a significant role in the formation of soil organic matter (SOM), but it is not clear how microbial traits influence residue accrual and SOM persistence. By pairing microbial biomarker and genomics approaches, we tested whether microbial life history strategies and residue accrual differed between primary (~70-year-old) and secondary (~30-year-old) subtropical forests. We found that microbial residue concentrations were significantly higher in secondary than primary forests, and strongly associated with several abundant microbial taxa (Ascomycota, Proteobacteria, Gemmatimonadetes). Microbial communities inhabiting resource-rich secondary forests were also associated with high growth yields and soil organic carbon (SOC) accrual (through residue retention), while nutrient-limited primary forests were dominated by microorganisms employing resource-acquisition strategies. We therefore suggest microbial life history traits can be used to link microbial community composition and metabolic processes with the turnover and transformation of SOC.
A substantial portion of grassland photosynthates is allocated belowground to arbuscular mycorrhizal fungi (AMF), but controversy remains about whether this carbon (C) contributes to soil organic carbon (SOC) under warming. The goal of this study was to investigate how AMF biomass and C sequestered by AMF (CNew) are influenced by soil warming. We estimated the AMF biomass and CNew, assumed to be mostly AMF necromass, in mycelial ingrowth bags buried for 1, 2, or 3 years in soil under warming (∼+0.5–16.4 °C). The AMF biomass had a positive, curvilinear response to warming gradients after one year of burial. About 107 g C m⁻² of CNew accumulated over the three years and ∼12% of this C was from glomalin-related soil protein. Modelling suggested the production rate of AMF biomass was 153 g C m⁻² yr⁻¹ with a rapid (36–75 days) turnover while AMF necromass turnover was much slower (1.4 ± 0.2 yr⁻¹). Warming duration (7–9 years vs. > 50 years) did not have significant influence on AMF biomass or CNew (P > 0.05). Our results suggest that AMF are more tolerant to increases in temperature than other microbes or fine roots. The dramatic loss of soil C and stable soil aggregates under warming found earlier at this site were not attributed to a decrease AMF biomass or CNew. Despite a low AMF standing biomass, its contribution to SOC may be substantial.
Soil organic matter (SOM) dynamics are central to soil biogeochemistry and fertility. The retention of SOM is governed initially by interactions with minerals, which mediate the sorption of chemically diverse organic matter (OM) molecules via distinct surface areas and chemical functional group availabilities. Unifying principles of mineral-OM interactions remain elusive because of the multi-layered nature of biochemical-mineral interactions that contribute to soil aggregate formation and the heterogeneous nature of soils among ecosystems. This study sought to understand how soil mineralogy as well as nitrogen (N) enrichment regulate OM composition in grassland soils. Using a multi-site grassland experiment, we demonstrate that the composition of mineral-associated OM depended on the clay content and specific mineral composition in soils across the sites. With increasing abundance of ferrihydrite (Fh) across six different grassland locations, OM in the hydrophobic zone became more enriched in lipid- and protein-like compounds, whereas the kinetic zone OM became more enriched in lignin-like molecules. These relationships suggest that the persistence of various classes of OM in soils may depend on soil iron mineralogy and provide experimental evidence to support conceptual models of zonal mineral-OM associations. Experimental N addition disrupted the accumulation of protein-like molecules in the hydrophobic zone and the positive correlation of lignin-like molecules in the kinetic zone with Fh content, compared to unfertilized soils. These data suggest that mineralogy and clay content together influence the chemical composition not only of mineral-associated OM, but also of soluble compounds within the soil matrix. If these relationships are prevalent over larger spatial and temporal scales, they provide a foundation for understanding SOM cycling and persistence under a variety of environmental contexts.
A process-based understanding of soil carbon (C) sequestration and stabilization has not been precisely characterized due to the lacking of linkage between microbial proliferation and mortality. In this study, stable isotope probing of phospholipid fatty acids and amino sugars were used to determine the microbial responses and microbial residue retention in two soils (Mollisol and Ultisol) with ¹³C-labeled glucose addition. The microbial responses stimulated by glucose were greater in C-poor Ultisol than in C-rich Mollisol. However, the transformation of labile C to microbial residues in Mollisol was more rapid. Therefore, the starvation effect may control microbial growth and microbial residue production, and thus resulting in distinct sequestration and stabilization process of labile C in different soils.
Understanding the processes controlling amino sugar accumulation in soil is essential for predicting the contribution of microbial residues to soil organic matter (SOM). The accumulation of amino sugars in soil is affected by multiple factors. Seldom are those factors examined together. We measured amino sugar concentration, extracellular enzyme activity, microbial respiration rate, and soil aggregate composition in an agricultural soil under 33-years of conservation management. The accumulation patterns of different amino sugars under the effects of no-tillage farming and cover cropping were compared and contrasted. The relative importance of physical, biochemical, and microbial controls of amino sugar accumulation was quantified using structural equation modelling. Our results show that although different types of amino sugars exhibited similar accumulation patterns in soil, their stabilization mechanisms might vary as demonstrated by structural equation models. The structural equation models indicate that macroaggregates had the largest total effect (0.59, P < 0.05) on muramic acid, and microbial respiration rate and wheat cover crops had large total effects (0.50 and −0.48 respectively, P < 0.05) on glucosamine. These results suggest that physical protection of soil aggregates played a critical role in muramic acid stabilization in soil, while microbial activity and nutrient condition were more critical for glucosamine. We also observed 24%–35% of decreases in soil amino sugars when nitrogen (N) was scarce and carbon (C) was excessive, concomitant with increases of extracellular enzyme activities. These results may support the theoretical model of microbial N mining. Structural equation model indicates that β-N-acetylglucosaminidase (NAG) had a negative effect on total amino sugars (−0.41, P < 0.05) and soil N had a negative effect on NAG (−0.27, P < 0.05). These results suggest that amino sugars can be decomposed by NAG as an alternative N source for microbes when readily available N was low. Leucine aminopeptidase (LAP) had a positive total effect on total amino sugars and a negative total effect on NAG (0.26 and −0.26 respectively, P < 0.05). This indicates that decomposition of amino acids by LAP may be a preferred strategy prior to decomposition of amino sugars by NAG to meet N requisition.
Microbial biomass turnover and the associated recycling of carbon (Cmic), nitrogen (Nmic) and phosphorus (Pmic) depend on their stoichiometric relationships and plays a pivotal role for soil fertility. This study examines the responses of Cmic, Nmic, Pmic, the microbial respiration rate (CO2 efflux), and the total DNA content to C and nutrient addition in forest soils with very low (Low-P) and high P (High-P) contents. Both the Low-P and High-P soils were treated with a low and high level of C, N and P (5% and 200% of Cmic, Nmic and Pmic). Phosphorus (33P) was added before the addition of C (14C) and N (15N) to investigate the potential P limitation. We hypothesized two modes of microbial biomass C and nutrient turnover: 1) maintenance through intracellular metabolisms and / or 2) microbial growth and death through necromass reutilization. In Low-P soil, the 2-day-sooner increase of Cmic and Pmic compared to the increase of CO2 efflux and DNA content after high CN input showed the rapid initial uptake of C and limiting nutrients into microbial cells. It also demonstrated a lag period before microbial growth commenced. In High-P soil, however, the CO2 efflux and DNA content increased simultaneously with increases in microbial biomass, reflecting the microbial capacity for immediate growth. Afterwards, CO2 efflux and DNA content dropped to the level before CNP addition, with a decline of Cmic and Pmic in Low-P soil and a decline of Nmic in High-P soil, suggesting a C and P limitation in Low-P soil and N limitation in High-P soil. Under low CNP addition, the microorganisms in High-P soil are ready to grow, while those in Low-P soil are mainly in maintenance mode. The microorganisms under maintenance in low-P soil can switch to growth/death mode after removing the nutrient limitation. High CNP input caused a non-homeostatic response of Cmic: Nmic: Pmic stoichiometry from 691:105:1 to 33:1:1 in Low-P soil, mainly resulting from a higher storage of the limiting elements (C and P) in microbial biomass. The ratio remained stable under low CNP addition due to the endogenous metabolism of C and nutrient at maintenance. The C and nutrient were turnovered much faster by microorganisms in the growth/death mode, confirming a key principle of ecology: the stronger the limitation by an element, the more efficiently that element is retained within an organism, and the more intensively it is reused. The triple labeling approach linked with Cmic: Nmic: Pmic stoichiometry helped to identify the dominant maintenance and growth/death modes of microbial biomass CNP turnover in nutrient-limited and -unlimited soil.
Despite recent progress in understanding soil microbial responses to carbon (C) limitation, the functional shifts in microbial community structure associated with decreasing soil C availability and changes in organic matter chemistry remain poorly known. It has been proposed that Gram-negative (GN) bacteria use more plant-derived C sources that are relatively labile, while Gram-positive (GP) bacteria use C sources derived from soil organic matter that are more recalcitrant. Because these two groups may differ in how they influence the fate of different C forms in soils, it is important to understand how they vary across ecosystems that differ in their vegetation cover and ecosystem productivity or across environmental gradients. In this study, we used a 19-year plant functional group removal experiment across a long term post-fire chronosequence to assess how microbial community structure (assessed using phospholipids fatty acids; PLFAs) and the association of bacterial functional groups (specifically, the GP:GN ratio) responded to changes in organic matter chemistry (measured via nuclear magnetic resonance; NMR). We found that the GP:GN ratio increased upon removal of shrubs and tree roots and with decreasing ecosystem productivity along the chronosequence, thus showing the greater dependence of GN than GP bacteria on more labile plant-derived C. Overall, GN bacteria were associated with simple C compounds (alkyls) whereas GP bacteria were more strongly associated with more complex C forms (carbonyls). Therefore,
we conclude that the GP:GN ratio has potential as a useful indicator of the relative C availability for soil bacterial communities in organic soils, and can be used as a coarse indicator of energy limitation in natural ecosystems.
Microbial residues play important role in regulating soil carbon (C) turnover and stability, but the responses of microbial residues to climate change are neglected. In this study, a 5-year field experiment that simulated two climate change factors (precipitation and warming) was performed to examine microbial residue changes in a semiarid grassland, with water limitation. Both the contents of total amino sugars (a biomarker of microbial residues) and glucosamine (a biomarker of fungal residues) increased significantly with increased precipitation and decreased under warming, whereas neither increased precipitation nor warming influenced the content of muramic acid (a biomarker of bacterial residues). These findings clarified the role of fungal residues in determining the response of microbial residues to altered water availability and plant productivity induced by increased precipitation and elevated temperature. Interestingly, microbial residues had a much greater response to climate change than total soil C, implying that soil C composition and stability altered prior to soil C storage and simultaneously slowed down the change of soil C pool. Integrating microbial residues into current climate-C models is expected to enable the models to more accurately evaluate soil C responses to climate regimes in semiarid grasslands.
The current review investigates the hypothesis that dormant soil microorganisms are relevant for microbial processes and community changes. Dormant soil microorganisms are C limited and do not grow. However, they still have a basic metabolism, which requires organic C uptake, resulting in a slow biomass turnover. Dormant soil microorganisms respond to substrate limitation by recycling own cell components and by down-regulating enzyme-expressing genes. The adsorption of microbial cells to clay and soil organic matter, intensified by limited water availability under unsaturated conditions, reduces microbial requirements for maintenance energy but causes immobility. For this reason, soil microorganisms cannot move rapidly towards places of demand for a certain microbial ability. Consequently, it can be assumed that subsoils and deeper vadose zone sediments must have been predominantly colonized by microorganisms during periods near to the surface, with access to autotrophic C inputs. Being remote from hotspots of C input, dormant microorganisms are an important reservoir of biodiversity and potential activity if an organic substrate arrives. The turnover of the whole microbial biomass C (MBC) is the product of C use efficiency (CUE) and a maintenance coefficient. For complex osmotrophic soil microbial communities, the CUE accounts for all biomass and metabolites synthesized during growth, i.e. especially exo-enzymes but also extracellular polymeric substances. This results in a mean CUE of 0.59 for easily soluble glucose and sucrose components and a mean CUE of 0.45 for more complex organic polymers such as cellulose, straw and MBC. The annual C input limits the MBC turnover time, which varies roughly around 365 days, assuming a CUE of 0.4 for soil organic matter.
Studies of the decomposition, transformation and stabilization of soil organic matter (SOM) have dramatically increased in recent years owing to growing interest in studying the global carbon (C) cycle as it pertains to climate change. While it is readily accepted that the magnitude of the organic C reservoir in soils depends upon microbial involvement, as soil C dynamics are ultimately the consequence of microbial growth and activity, it remains largely unknown how these microorganism-mediated processes lead to soil C stabilization. Here, we define two pathways—ex vivo modification and in vivo turnover—which jointly explain soil C dynamics driven by microbial catabolism and/or anabolism. Accordingly, we use the conceptual framework of the soil ‘microbial carbon pump’ (MCP) to demonstrate how microorganisms are an active player in soil C storage. The MCP couples microbial production of a set of organic compounds to their further stabilization, which we define as the entombing effect. This integration captures the cumulative long-term legacy of microbial assimilation on SOM formation, with mechanisms (whether via physical protection or a lack of activation energy due to chemical composition) that ultimately enable the entombment of microbial-derived C in soils. We propose a need for increased efforts and seek to inspire new studies that utilize the soil MCP as a conceptual guideline for improving mechanistic understandings of the contributions of soil C dynamics to the responses of the terrestrial C cycle under global change.
The immense diversity of microbial life found in the vadose zone reflects the extremely heterogeneous and highly dynamic aquatic and chemical environments formed within soil pore spaces. The notion of planktonian free swimming microbes is unrealistic under most unsaturated conditions. Experimental and theoretical evidence suggests that surface attachment is the prevailing lifestyle, where bacterial colonies are embedded in biosynthesized extracellular polymeric substances (EPS). This strategy represents a successful adaptation to the variable and unpredictable hydration conditions near the earth surface. The EPS matrix serves as the interface with the environment; it enhances hydration and transport properties in the immediate vicinity of microbial cells, and dampens effects of highly transient fluctuations in water and nutrient fluxes. The primary effect of soil pore geometry and hydration status is on diffusion pathways to and away from stationary microbial colonies. Microbial dependency on diffusion processes occurs at all scales, but is particularly important at the colony scale. We illustrate the critical role of diffusion pathways with their complex spatial and temporal patterns in promoting coexistence and diversity. We review specific features and adaptations of microbial life to the particular conditions of terrestrial soil environments. The physical and related chemical conditions that shape microbial habitats and govern key processes in unsaturated soils are reviewed in a quantitative framework. Key physiological adaptations and biological responses to challenges presented by unsaturated conditions are discussed. Finally, we discuss potential impacts of microbial activity on properties and characteristics of the host porous medium. This review is an attempt to establish an interdisciplinary dialogue between hydrologists and microbiologists towards a quantitative integration of the role of hydrologic conditions on microbial activity and the role of microbiology in controlling macroscopic fluxes within this important compartment of the biosphere.
Profiling of microbial communities in environmental samples often utilizes phospholipid fatty acid (PLFA) analysis. This method has been used for more than 35 years and is still popular as a means to characterize microbial communities in a diverse range of environmental matrices. This review examines the various recent applications of PLFA analysis in environmental studies with specific reference to the interpretation of the PLFA results. It is evident that interpretations of PLFA results do not always correlate between different investigations. These discrepancies in interpretation and their subsequent applications to environmental studies are discussed. However, in spite of limitations to the manner in which PLFA data is applied, the approach remains one with great potential for improving our understanding of the relationship between microbial populations and the environment. This review highlights the caveats and provides suggestions towards the practicable application of PLFA data interpretation. This article is protected by copyright. All rights reserved.
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[1] Carbon isotopes are applied to estimate soil decomposition and physical mixing in well-drained forest soils by coupling new isotope and soil organic carbon (SOC) data with literature meta-analysis and carbon isotope mass balance modeling. New soil data results are presented for old- and second-growth forests in Southern Appalachia, USA and the Blue Mountains, Australia. The soils exhibit a SOC decrease and δ13C increase with depth. The regressed gradient, termed β, of δ13C and the logarithm of SOC with depth in the soil column ranged from −1.09 to −1.65 for the measured soils. Twenty-four soils from 11 published studies across a range of cool temperate to tropical forest soils are used to show that β is dependent upon mean annual temperature (MAT) alone as well as mean annual temperature, mean annual precipitation, and soil texture, thus connecting the natural (nonlabeled) carbon isotope signature to the soil factors controlling soil decomposition and physical mixing. Carbon elemental and isotopic mass balance modeling of multiple SOC pools and multiple soil depths suggest that rates of decomposition and mixing are of the same order of magnitude for turnover in the studied forest soils. The results support the hypothesis that a pronounced negative, regressed β is indicative of isotopic fractionation during decomposition and physical mixing processes that occurs during soil turnover, and other hypotheses posed in the literature are marginalized using modeling and discussion. We discuss integration of the isotope method with existing SOC turnover models as a future research avenue.
Amino sugars are one of the important microbial residue biomarkers which are associated with soil organic matter cycling. However, little is known about their transformation kinetics in response to available substrates because living biomass only contributes a negligible portion to the total mass of amino sugars. By using 15N tracing technique, the newly synthesized (labeled) amino sugars can be differentiated from the native portions in soil matrix, making it possible to evaluate, in quantitative manner, the transformation pattern of amino sugars and to interpret the past and ongoing changes of microbial communities during the assimilation of extraneous 15N. In this study, laboratory incubations of soil samples were conducted by using 15NH4+ as nitrogen source with or without glucose addition. Both the 15N enrichment (expressed as atom percentage excess, APE) and the contents of amino sugars were determined by an isotope-based gas chromatography–mass spectrometry. The significant 15N incorporation into amino sugars was only observed in glucose plus 15NH4+ amendment with the APE arranged as: muramic acid (MurN) > glucosamine (GlcN) > galactosamine (GalN). The dynamics of 15N enrichment in bacterial-derived MurN and fungal-derived GlcN were fitted to the hyperbolic equations and indicative for the temporal responses of different soil microorganisms. The APE plateau of MurN and fungal-derived GlcN represented the maximal extent of bacterial and fungal populations, respectively, becoming active in response to the available substrates. The different dynamics of the 15N enrichment between MurN and GlcN indicated that bacteria reacted faster than fungi to assimilate the labile substrates initially, but fungus growth was dominant afterward, leading to integrated microbial community structure over time. Furthermore, the dynamics of labeled and unlabeled portions of amino sugars were compound-specific and substrate-dependent, suggesting their different stability in soil. GlcN tended to accumulate in soil while MurN was more likely degraded as a carbon source when nitrogen supply was excessive.
An incubation experiment with organic soil amendments was carried out with the aim to determine whether formation and use of microbial tissue (biomass and residues) could be monitored by measuring glucosamine and muramic acid. Living fungal tissue was additionally determined by the cell-membrane component ergosterol. The organic amendments were fibrous maize cellulose and sugarcane sucrose adjusted to the same C/N ratio of 15. In a subsequent step, spherical cellulose was added without N to determine whether the microbial residues formed initially were preferentially decomposed. In the non-amended control treatment, ergosterol remained constant at 0.44 μg g−1 soil throughout the 67-day incubation. It increased to a highest value of 1.9 μg g−1 soil at day 5 in the sucrose treatment and to 5.0 μg g−1 soil at day 33 in the fibrous cellulose treatment. Then, the ergosterol content declined again. The addition of spherical cellulose had no further significant effects on the ergosterol content in these two treatments. The non-amended control treatment contained 48 μg muramic acid and 650 μg glucosamine g−1 soil at day 5. During incubation, these contents decreased by 17% and 19%, respectively. A 33% increase in muramic acid and an 8% increase in glucosamine were observed after adding sucrose. Consequently, the ratio of fungal C to bacterial C based on bacterial muramic acid and fungal glucosamine was lowered in comparison with the other two treatments. No effect on the two amino sugars was observed after adding cellulose initially or subsequently during the second incubation period. This indicates that the differences in quality between sucrose and cellulose had a strong impact on the formation of microbial residues. However, the amino sugars did not indicate a preferential decomposition of microbial residues as N sources.
Microbial digestive enzymes in soil and litter have been studied for over a half century, yet the understanding of microbial enzymes as drivers of ecosystem processes remains hindered by methodological differences among researchers and laboratories. Modern techniques enable the comparison of enzyme activities from different sites and experiments, but most researchers do not optimize enzyme assay methods for their study sites, and thus may not properly assay potential enzyme activity. In this review, we characterize important procedural details of enzyme assays, and define the steps necessary to properly assay potential enzyme activities in environmental samples. We make the following recommendations to investigators measuring soil enzyme activities: 1) run enzyme assays at the environmental pH and temperature; 2) run proper standards, and if using fluorescent substrates with NaOH addition, use a standard time of 1 min between the addition of NaOH and reading in a fluorometer; 3) run enzyme assays under saturating substrate concentrations to ensure Vmax is being measured; 4) confirm that product is produced linearly over the duration of the assay; 5) examine whether mixing during the reaction is necessary to properly measure enzyme activity; 6) find the balance between dilution of soil homogenate and assay variation; and 7) ensure that enzyme activity values are properly calculated. These steps should help develop a unified understanding of enzyme activities in ecosystem ecology.
We assessed the contribution of polysaccharides and lignin, major components of plant residues, to the refractory pool of soil organic carbon (SOC) in arable soils. Soil samples from two contrasting treatment types of European long-term agroecosystem experiments, i.e. conventionally managed (fertilized) and C-depleted plots, enriched in refractory compounds, were compared. Bulk samples from eight experimental sites and particle-size fractions of two of the sites were investigated. The CuO oxidation technique was used as a relative measure of lignin and its degree of structural alteration. The contents and composition of polysaccharides were determined following hydrolysis with trifluoroacetic acid (TFA). For the bulk samples, the amount of lignin phenols declined more than the total OC in the course of C-depletion. The contribution of lignin phenols to total OC was thus lower in the C-depleted versus the fertilized plots. A greater lignin biodegradation was found in the bulk samples of the depleted plots compared with the fertilized plots. The analysis of size fractions revealed lower OC-normalized contents of lignin phenols and a higher degree of lignin alteration in fractions