Article

Dominant influence of plants on soil microbial carbon cycling functions during natural restoration of degraded karst vegetation

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Abstract

The impacts of natural restoration projects on soil microbial carbon (C) cycling functions have not been well recognized despite their wide implementation in the degraded karst areas of southwest China. In this study, metagenomic sequencing assays were conducted on functional genes and microorganisms related to soil C-cycling at three natural restoration stages (shrubbery, TG; secondary forest, SG; old-growth forest, OG) in the southeast of Guizhou Province, China. The aims were to investigate the changes in microbial potentials responsible for soil C cycling and the underlying driving forces. The natural restoration resulted in vegetation establishment at all three restoration stages, rendering alterations of soil microbial C cycle functions as indicated by metagenomic gene assays. When TG was restored into OG, the number and diversity of genes and microorganisms involved in soil C cycling remained unchanged, but their composition underwent significant shifts. Specifically, microbial potentials for soil C decomposition exhibited an increase driven by the collaborative efforts of plants and soils, while microbial potentials for soil C biosynthesis displayed an initial upswing followed by a subsequent decline which was primarily influenced by plants alone. In comparison to soil nutrients, it was determined that plant diversities served as the primary driving factor for the alterations in microbial carbon cycle potentials. Soil microbial communities involved in C cycling were predominantly attributed to Proteobacteria (31.87%-40.25%) and Actinobacteria (11.29%-26.07%), although their contributions varied across the three restoration stages. The natural restoration of degraded karst vegetation thus influences soil microbial C cycle functions by enhancing C decomposition potentials and displaying a nuanced pattern of biosynthesis potentials, primarily influenced by above-ground plants. These results provide valuable new insights into the regulation of soil C cycling during the restoration of degraded karst vegetation from genetic and microbial perspectives.

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... The Karst Mountains of Southwestern China, spanning approximately 540,000 km 2 , represent one of the most extensive continuous karst landscapes globally [1]. This region has experienced profound losses in agricultural and forestry productivity, alongside drastic declines in plant diversity, soil physicochemical characteristics, microbial diversity, and carbon sequestration capacity [2][3][4]. These changes are attributed to a variety of natural and human-induced disturbances, rendering it one of the areas most severely impacted by rocky desertification [5]. ...
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Background Evergreen coniferous forests contain high stocks of organic matter. Significant carbon transformations occur in litter and soil of these ecosystems, making them important for the global carbon cycle. Due to seasonal allocation of photosynthates to roots, carbon availability changes seasonally in the topsoil. The aim of this paper was to describe the seasonal differences in C source utilization and the involvement of various members of soil microbiome in this process. Results Here, we show that microorganisms in topsoil encode a diverse set of carbohydrate-active enzymes, including glycoside hydrolases and auxiliary enzymes. While the transcription of genes encoding enzymes degrading reserve compounds, such as starch or trehalose, was high in soil in winter, summer was characterized by high transcription of ligninolytic and cellulolytic enzymes produced mainly by fungi. Fungi strongly dominated the transcription in litter and an equal contribution of bacteria and fungi was found in soil. The turnover of fungal biomass appeared to be faster in summer than in winter, due to high activity of enzymes targeting its degradation, indicating fast growth in both litter and soil. In each enzyme family, hundreds to thousands of genes were typically transcribed simultaneously. Conclusions Seasonal differences in the transcription of glycoside hydrolases and auxiliary enzyme genes are more pronounced in soil than in litter. Our results suggest that mainly fungi are involved in decomposition of recalcitrant biopolymers in summer, while bacteria replace them in this role in winter. Transcripts of genes encoding enzymes targeting plant biomass biopolymers, reserve compounds and fungal cell walls were especially abundant in the coniferous forest topsoil. Electronic supplementary material The online version of this article (10.1186/s40168-017-0340-0) contains supplementary material, which is available to authorized users.
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Diversity and community composition of soil microorganisms along the elevation climosequences have been widely studied, while the microbial metabolic potential, particularly in regard to carbon (C) cycling, remains unclear. Here, a metagenomic analysis of C related genes along five elevations ranging from 767 to 4190 m at Mount Kilimanjaro was analysed to evaluate the microbial organic C transformation capacities in various ecosystems. The highest gene abundances for decomposition of moderate mineralizable compounds, i.e. carbohydrate esters, chitin and pectin were found at the mid-elevations with hump-shaped pattern, where the genes for decompositions of recalcitrant C (i.e. lignin) and easily mineralizable C (i.e. starch) showed the opposite trend (i.e. U-shaped pattern), due to high soil pH and seasonality in both low and high elevations. Notably, the gene abundances for the decompositions of starch, carbohydrate esters, chitin and lignin had positive relationships with corresponding C compounds, indicating the consistent responses of microbial functional profiles and metabolites to elevation climosequences. Understanding of adaptation of microbial communities, potential function and metabolites to elevation climosequences and their influencing factors provided a new insight for the regulation of terrestrial C storage.
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Forest soils represent important terrestrial carbon (C) pools, where C is primarily fixed in plant biomass and then is incorporated in the biomass of fungi and bacteria. Although classical concepts assume that fungi are the main decomposers of the recalcitrant organic matter within plant and microbial biomass, whereas bacteria are considered to mostly utilize simpler compounds, recent studies have shown that fungi and bacteria overlap in substrate utilization. Here, we studied the microbial contribution to the recycling of dead biomass by analyzing the bacterial and fungal communities in soil microcosms supplemented with ¹³C-labeled biomass of plant, fungal, and bacterial origin using a combination of DNA-stable isotope probing and metagenomics. Both fungi and bacteria contributed actively to the degradation of complex components of plant and microbial biomass. Specific families of carbohydrate-active enzymes (CAZyme) were involved in the degradation of each biomass type. Moreover, the analysis of five bacterial metagenome-assembled genomes indicated the key role of some bacterial genera in the degradation of plant biomass (Cytophaga and Asticcacaulis) and microbial biomass (Herminiimonas). The enzymatic systems utilized by bacteria are highly complex and complementary but also highly diverse among taxa. The results confirm the importance of bacteria, in addition to fungi, as decomposers of complex organic matter in forest soils.
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Ecosystem functional responses such as soil CO 2 emissions are constrained by microclimate, available carbon (C) substrates and their effects upon microbial activity. In tropical forests, phosphorus (P) is often considered as a limiting factor for plant growth, but it is still not clear whether P constrains microbial CO 2 emissions from soils. In this study, we incubated seven tropical forest soils from Brazil and Puerto Rico with different nutrient addition treatments (no addition, Control; C, nitrogen (N) or P addition only; and combined C, N and P addition (CNP)). Cumulative soil CO 2 emissions were fit with a Gompertz model to estimate potential maximum cumulative soil CO 2 emission ( C m ) and the rate of change of soil C decomposition ( k ). Quantitative polymerase chain reaction (qPCR) was conducted to quantify microbial biomass as bacteria and fungi. Results showed that P addition alone or in combination with C and N enhanced C m , whereas N addition usually reduced C m , and neither N nor P affected microbial biomass. Additions of CNP enhanced k , increased microbial abundances and altered fungal to bacterial ratios towards higher fungal abundance. Additions of CNP, however, tended to reduce C m for most soils when compared to C additions alone, suggesting that microbial growth associated with nutrient additions may have occurred at the expense of C decomposition. Overall, this study demonstrates that soil CO 2 emission is more limited by P than N in tropical forest soils and those effects were stronger in soils low in P. Highlights A laboratory incubation study was conducted with nitrogen, phosphorus or carbon addition to tropical forest soils. Soil CO 2 emission was fitted with a Gompertz model and soil microbial abundance was quantified using qPCR. Phosphorus addition increased model parameters C m and soil CO 2 emission, particularly in the Puerto Rico soils. Soil CO 2 emission was more limited by phosphorus than nitrogen in tropical forest soils.
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Bacteria belong to the key players in the carbon cycling in forest soils and thus affect the global C balance. Our understanding of bacterial contribution to ecosystem processes relies on the analysis of whole communities. Here we combined strain isolation, genome sequencing and metatranscriptomics to analyse the activity of individual bacterial species in the topsoil of a temperate coniferous forest. Our results show that transcription profiles in litter and soil differ, indicating that bacterial activity is shaped by their habitat. Importantly, transcript pools also significant differ between summer when primary producers are active and winter. We show that Acidobacteria and Bacteroidetes with high metabolic capacity for polysaccharide decomposition in their genomes actively transcribe corresponding genes in situ. The rate of the transcription of ribosomal proteins, a proxy of growth, seasonally differs between these “decomposer” taxa and other “opportunistic” bacteria. While the former grow at similar rates in summer and winter, the latter grow much faster in summer when labile C, delivered by plant roots, is available. This paper demonstrates differences in activity of bacterial guilds as well as the importance of environmental drivers for the activity of individual bacteria.
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Grassland afforestation strongly influences the structure and function of soil microorganisms. Yet the mechanisms of how afforestation could simultaneously alter both the soil fungal and bacterial communities and its implications for ecosystem management are poorly understood, especially in nitrogen-limited ecosystems. Using high-throughput sequencing of 16S rRNA and ITS rRNA genes, the present study investigated the changes in soil properties and soil microorganisms after afforestation of natural grasslands with Chinese pine (Pinus tabuliformis)on the Loess Plateau in China. Results showed that soil bacterial diversity had no significant differences among the grassland (GL), forest–grassland transition zone (TZ), and forestland (FL), while soil fungal diversity in the GL was significantly higher than that in the FL and TZ (P < 0.05). The proportion of shared OTUs in the soil bacterial community was higher than that in the soil fungal community among the three land use types. The dominant bacterial phylum shifted from Proteobacteria to Actinobacteria, while the dominant fungal phylum shifted from Ascomycota to Basidiomycota after the GL conversion to the FL. The functional groups of ECM fungi increased significantly while biotrophic fungi decreased significantly after grassland afforestation. Both the soil bacterial and fungal communities in the TZ showed great similarity with those in the FL. In addition, among all examined soil properties, soil nitrogen (N)showed a more significant effect on the soil microbial communities. The reduction of soil N after grassland afforestation resulted in both the structure and function changes in soil microbial communities. Our results demonstrated simultaneously differential changes in the composition and diversity of both soil bacterial and fungal communities after afforestation from grasslands to planted forests.
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Natural regeneration and reforestation have been widely adopted to improve the degraded soil and promote ecological services in the karst regions of southwestern China. A better understanding the effects of different vegetation types on soil quality and the nutrient limiting factors is very important for each approach. In this study, a secondary forest (SF) and two plantations, Eucalyptus maideni F. V. Muell. (EM, exotic, deciduous broad-leaved) and Pinus yunnanensis Franch. (PY, native, conifer species), were selected in the karst graben basins of southwest China to explore the soil quality using Total Data Set (TDS) and Minimum Data Set (MDS) methods. The results indicated most soil parameters showed significant differences between the different recovery approaches. The TDS method is more precise than the MDS method, but the MDS method can also adequately represent the TDS method for the evaluation of soil quality with different vegetation restoration schemes. In the MDS method, soil organic carbon, available potassium, ammonium nitrogen, acid phosphatase, microbial metabolic quotient, and the Pielou index of the soil microbes were found to be the most important indicators for assessing soil quality. The pure plantation of PY had a negative effect on the soil quality, causing soil nutrient deficiency, compared to the SF and EM plantation, indicating that natural regeneration may be a more effective approach to the amelioration of soil quality in the karst areas. These findings provide an empirical and theoretical basis for the protection, restoration, and management of forest in the degraded karst areas.
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To elucidate the effects of land-use types and afforestation age on litter decomposition, soil nutrient dynamics, and their relationship with substrate quality and soil environmental conditions, soil and litter samples were collected from farmland as well as four afforested land-use types (Robinia pseudoacacia: Rps; Caragana korshinskii: Cko; Pinus tabulaeformis: Pta; and Armeniaca sibirica: Asi), with each land-use type having three succession chronosequences (10, 25, and 40 a) in the Gaoxigou catchment area. These twelve afforested lands were converted from similar farmlands, and litterbag experiments were conducted in each land to determine litter decomposition rate (LDR). In addition, the carbon, nitrogen, and phosphorus contents and stoichiometry in soil and litter, soil properties, and litter biomass were determined. The results showed that soil environmental conditions such as soil water content, bulk density, pH, and temperature improved with afforestation age. Soil nutrient contents were higher in afforested lands and increased with afforestation age. The soil organic carbon (OC), total nitrogen (TN), and total phosphorus (TP) were positively correlated with the litter biomass, soil microbial carbon, and soil water content, but were negatively correlated with the soil bulk density, pH, and temperature. The litter OC, TN, and TP contents were mainly affected by the land-use types without being influenced by afforestation age. LDR is the main litter factor affecting soil nutrients, and is significantly influenced by substrate quality and environmental conditions, especially litter TN and N:P ratio, soil water content, and pH. The annual rates of increase for soil OC and TN during the initial (farmland–10a) and middle (10–25 a) periods were significantly higher than those during the later period (25–40 a) in Rps and Cko, but the Pta forest showed a completely opposite trend, which can be explained by a synchronous change in the LDR driven by the soil water content. In addition, the soil OC, TN, and TP contents were positively correlated with the litter TN, TP, and biomass, but had no correlation with the litter OC. The N:P ratio can be used as an indicator to reveal a tight coupling among soil and litter nutrients. Overall, these results provide evidence that litter decomposition in afforestation systems is linked to soil nutrient dynamics, and is mainly limited by substrate quality and environmental conditions.
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Forest soils represent important terrestrial carbon (C) pools where C is primarily fixed in the plant-derived biomass but it flows further through the biomass of fungi and bacteria before it is lost from the ecosystem as CO2 or immobilized in recalcitrant organic matter. Microorganisms are the main drivers of C flow in forests and play critical roles in the C balance through the decomposition of dead biomass of different origins. Here, we track the path of C that enters forest soil by following respiration, microbial biomass production, and C accumulation by individual microbial taxa in soil microcosms upon the addition of 13C-labeled biomass of plant, fungal, and bacterial origin. We demonstrate that both fungi and bacteria are involved in the assimilation and mineralization of C from the major complex sources existing in soil. Decomposer fungi are, however, better suited to utilize plant biomass compounds, whereas the ability to utilize fungal and bacterial biomass is more frequent among bacteria. Due to the ability of microorganisms to recycle microbial biomass, we suggest that the decomposer food web in forest soil displays a network structure with loops between and within individual pools. These results question the present paradigms describing food webs as hierarchical structures with unidirectional flow of C and assumptions about the dominance of fungi in the decomposition of complex organic matter.
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Soil microorganisms are clearly a key component of both natural and managed ecosystems. Despite the challenges of surviving in soil, a gram of soil can contain thousands of individual microbial taxa, including viruses and members of all three domains of life. Recent advances in marker gene, genomic and metagenomic analyses have greatly expanded our ability to characterize the soil microbiome and identify the factors that shape soil microbial communities across space and time. However, although most soil microorganisms remain undescribed, we can begin to categorize soil microorganisms on the basis of their ecological strategies. This is an approach that should prove fruitful for leveraging genomic information to predict the functional attributes of individual taxa. The field is now poised to identify how we can manipulate and manage the soil microbiome to increase soil fertility, improve crop production and improve our understanding of how terrestrial ecosystems will respond to environmental change.
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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.
Article
This study was aimed to investigate the direction and magnitude of soil organic carbon (SOC) dynamics and the underlying mechanisms following agricultural abandonment in a subtropical karst area, southwest China. Two post-agriculture succession sequences including grassland (~10 years), shrubland (~29 years), secondary forest (~59 years) and primary forest with cropland as reference were selected. SOC and other soil physicochemical variables in the soil depth of 0–15 cm (representing the average soil depth of the slope in the studied area) were measured. SOC content in the grassland was not significantly elevated relative to the cropland (42.0 ± 7.3 Mg C ha⁻¹). SOC content in the shrubland reached the level of the primary forest. On average, SOC content for the forest was 92.6 ± 4.2 Mg C ha⁻¹, representing an increase of 120.4 ± 10.0% or 50.6 ± 4.2 Mg ha⁻¹ relative to the cropland. Following agricultural abandonment, SOC recovered to the primary forest level in about 40 years with a rate of 1.38 Mg C ha⁻¹ yr⁻¹. Exchangeable Ca and Mg were found to be the strongest predictors of SOC dynamics. Our results suggest that SOC content may recover rapidly following agricultural abandonment in the karst region of southwest China.
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Polysaccharide lyases are the products of various microorganisms, bacteriophage and some eukaryotes. All such enzymes cleave a hexose‐1,4‐α‐ or β‐uronic acid sequence by β‐elimination. They are in some examples, the only known type of enzymes degrading their polyanionic substrates. Although only a small number of these enzymes have been exhaustively studied, the pectin lyases of bacterial origin have proved to be of interesting crystal structure containing a parallel β‐helix domain. Alginate and heparin lyases may yield products with biotechnological potential.
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The effects of natural succession on plant communities and soil variables have been established, but changes in microbial communities and their response to plants and soils have not been well characterized in secondary succession. We investigated the changes in soil properties and plant and soil microbial communities during the secondary succession on abandoned cropland in the Loess Plateau of China using high-throughput sequencing of the 16S rRNA gene. The study analyzed a chronosequence of farmland undergoing spontaneous succession after being abandoned for 0 (farmland), 5, 10, 15, 20 and 30 years(y). Plant community metrics including percent cover, and above/belowground biomass, first decreased in the initial stage (<10 y) and then increased during the succession. Proteobacteria, Acidobacteria, and Actinobacteria were the dominant phyla of soil bacteria across all succession. Bacterial communities transitioned from Acidobacteria-dominant to Proteobacteria-dominant communities during the 30 years of succession. Levels of soil organic carbon (C), total nitrogen (N), nitrate N and bacterial diversity were lower soon (<5 years) after abandonment compared to the farmland, but they could recover to farmland levels after 15–20 years and were much improved after continued succession. Plant and bacterial community diversities (Shannon index and species richness) changed along successional time, but they showed different patterns, suggesting an incongruous process between plant and microbial succession. Organic C, total N, available N, and available P contents were significantly correlated with the abundance of most bacterial groups and the Shannon index, indicating the dependence of bacterial community diversity on soil nutrient supply.