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Relationships between oxalic acid and soil total nitrogen in rhizosphere soils of shrubs and trees. ○ shrubs, non-growing season; ● shrubs, growing season; △ trees, non-growing season; ▲ trees, growing season; black and red regression lines are for shrubs and trees, respectively; ∗∗∗p < 0.001.
Source publication
In karst ecosystems, a high level of CaCO3 enhances the stabilization of soil organic matter (SOM) and causes nitrogen (N) and/or phosphorus (P) limitation in plants. Oxalic acid has been suggested to be involved in the nutrient-acquisition strategy of plants because its addition can temporarily relieve nutrient limitation. Therefore, understanding...
Citations
... Community assembly describes how different ecological processes shape the composition and structure of microbial communities (Ning et al., 2024). Studying the effects of environmental factors on the assembly of microbial communities is critical to understanding microbial biodiversity and ecological All values are reported as "mean ± standard deviation" based on measurement results for samples. ...
Karst rocky desertification refers to the process of land degradation caused by various factors such as climate change and human activities including deforestation and agriculture on a fragile karst substrate. Nutrient limitation is common in karst areas. Moss crust grows widely in karst areas. The microorganisms associated with bryophytes are vital to maintaining ecological functions, including climate regulation and nutrient circulation. The synergistic effect of moss crusts and microorganisms may hold great potential for restoring degraded karst ecosystems. However, our understanding of the responses of microbial communities, especially abundant and rare taxa, to nutrient limitations and acquisition in the presence of moss crusts is limited. Different moss habitats exhibit varying patterns of nutrient availability, which also affect microbial diversity and composition. Therefore, in this study, we investigated three habitats of mosses: autochthonal bryophytes under forest, lithophytic bryophytes under forest and on cliff rock. We measured soil physicochemical properties and enzymatic activities. We conducted high-throughput sequencing and analysis of soil microorganisms. Our finding revealed that autochthonal moss crusts under forest had higher nutrient availability and a higher proportion of copiotrophic microbial communities compared to lithophytic moss crusts under forest or on cliff rock. However, enzyme activities were lower in autochthonal moss crusts under forest. Additionally, rare taxa exhibited distinct structures in all three habitats. Analysis of co-occurrence network showed that rare taxa had a relatively high proportion in the main modules. Furthermore, we found that both abundant and rare taxa were primarily assembled by stochastic processes. Soil properties significantly affected the community assembly of the rare taxa, indirectly affecting microbial diversity and complexity and finally nutrient acquisition. These findings highlight the importance of rare taxa under moss crusts for nutrient acquisition. Addressing this knowledge gap is essential for guiding ongoing ecological restoration projects in karst rocky desertification regions.
... In total, 18 plots (two type forests × nine replicate plots) were established. The dominant understory species in karst forests included Celtis biondii (Cannabaceae), Cleidion bracteosum (Euphorbiaceae), Cryptocarya chinensis (Lauraceae), Cyclobalanopsis glauca (Fagaceae), Loropetalum chinense (Hamamelidaceae), Miliusa chunii (Annonaceae), and Pteroceltis tatarinowii (Cannabaceae) [34,35]. The dominant understory species in non-karst forests included Pinus massoniana These two types of forests were approximately 30 years old, according to the reserve materials of the Mulun Reserve and Huashan Forest Farm, and originated from the natural restoration of forests after returning farmland (mainly used for growing corn) to forests. ...
... In total, 18 plots (two type forests × nine replicate plots) were established. The dominant understory species in karst forests included Celtis biondii (Cannabaceae), Cleidion bracteosum (Euphorbiaceae), Cryptocarya chinensis (Lauraceae), Cyclobalanopsis glauca (Fagaceae), Loropetalum chinense (Hamamelidaceae), Miliusa chunii (Annonaceae), and Pteroceltis tatarinowii (Cannabaceae) [34,35]. The dominant understory species in non-karst forests included Pinus massoniana (Pinaceae), Schefflera heptaphylla (Araliaceae), Ficus tikoua (Moraceae), Vernonia solanifolia (Asteraceae), Evodia lepta (Rutaceae), and Rhodomyrtus tomentosa (Myrtaceae) [36]. ...
... According to the two standards, eight OTUs were identified as core functional bacteria: the karst forest soils contained Burkholderiales OTUs (13,132,154,158) and unclassified Proteobacteria OTUs (21,144,194,34) (Figure 6a). The non-karst forest soils contained the Burkholderiale OTU 63), Rhizobiales OTUs (13539, 69, 99, and 80), and unclassified Proteobacteria OTUs (40,383,51) (Figure 6b). ...
Phosphorous (P) limitation is common not only in tropical rainforest and savanna ecosystems, but also in karst forest ecosystems. Soil phoD-harboring microorganisms are essential in soil P cycles, but very little information is available about them in karst ecosystems. A total of 36 soil samples were collected from two types of forest ecosystems (karst and non-karst) over two seasons (rainy and dry), and the diversity and community structure of soil phoD-harboring microorganisms were measured. The contents of available P (AP), soil total P (TP), microbial biomass P (MBP) and the activity of alkaline phosphatase (ALP) in karst forest soils were higher than those in non-karst forest soils, whereas the contents of CaCl2-P, citrate-P, enzyme-P and the activity of acid phosphatase (ACP) were the opposite. Soil AP content was significantly higher in the rainy season than in the dry season, whereas ALP activity was the opposite. The community structure of phoD-harboring microorganisms was more influenced by forest-type than season. The network connectivity was higher in non-karst forests than in karst forests. Two dominant orders, Burkholderiales and Rhizobiales, were the keystone taxa in these networks in two forests, and their relative abundances were higher in non-karst forests than in karst forests. The microorganic diversity indices (e.g., Shannon–Wiener, Evenness, Richness, and Chao1) were substantially higher in karst than in non-karst forests. These indices were positively correlated with the contents of SOC and TN in the two forests; meanwhile, richness and evenness indices were positively correlated with citrate-P, HCl-P, and TP in non-karst forests. Structural equation modelling results showed that the relative abundance of phoD-harboring microorganisms was mainly influenced by pH and AP, with direct affection of soil AP, pH, and ALP activity, and indirect affection of ALP activity through affecting AP. These findings highlight that the P cycle is mainly regulated by the diversity of phoD-harboring microorganisms in karst forest ecosystems, whereas it is mainly regulated by dominant taxa in non-karst forest ecosystems. In future, regulating the interaction networks and keystone taxa of phoD-harboring microorganisms may be critical to alleviating P limitations in karst forest ecosystems.
... Soils in karst ecosystems are characterized by high pH and calcium (Ca) content. This results in large amounts of P stabilized by directly binding Ca and through the formation of Ca bridges in the soil organic matter (Clarholm et al., 2015;Pan et al., 2016;Liang et al., 2022). Therefore, although karst ecosystems tend to have higher total P content, plant growth in these ecosystems is more restricted by soil P availability compared with that in nonkarst ecosystems. ...
... However, recent emerging studies of biogeochemical cycling implied that roots and associated mycelia may play a vital role in destabilizing physicochemically protected N compounds (Li et al. 2021; Thorley et al. 2014). This effect is because root-and mycelia-derived C fluxes contain approximately 10% of total dissolved C as low-molecular-weight organic acids (LMWOAs) (van Hees and Lundström, 2008;Pan et al. 2016) that can complex with protective metals in soils (Clarholm et al. 2015). ...
... Therefore, plant roots and mycelia may play a vital but distinct role in disrupting the stability of physicochemically protected N compounds via their release of LMWOAs (Li et al. 2021;Thorley et al. 2014), which causes different amounts of nitrogenous compounds to become accessible to microbial and enzymatic decomposition (Clarholm et al. 2015;Li et al. 2021). Although the critical role of rhizosphere processes in soil N mineralization is well recognized (Finzi et al. 2015), our understanding of how plant roots and mycelia enhance soil N mineralization through biotic and abiotic mechanisms remains limited but is essential for understanding N cycling, especially in karst forests where soil nutrient availability is relatively limited (Hao et al. 2019;Pan et al. 2016). ...
PurposePlant roots and associated mycelia play a crucial role in soil nitrogen (N) cycling. However, the underlying mechanisms by which roots and mycelia affect soil N transformation in karst soil remain unclear.Methods
By using ingrowth cores, the present study focused on elucidating the underlying mechanisms by which roots and mycelia impact soil N transformation in a Cryptomeria fortune plantation in a karst region.ResultsBoth roots and mycelia significantly increased the net N mineralization rate, with increases in magnitude of 9% and 25%, respectively, in soils of the Cryptomeria fortune plantation. Moreover, we found that this increase in N mineralization coincided with significant increases in the microbial biomass and extracellular enzyme activities, suggesting that both roots and mycelia could enhance N mineralization through their effect on microbial processes. Moreover, mycelia induced a significant decrease in metal-mineral organic complexes, on which roots had only a minor net effect, implying that mycelia could enhance N mineralization via their effects on the breakage of mineral-associated N complexes.Conclusions
These combined results suggest that plant roots and mycelia accelerate soil N transformation through different mechanisms. In particular, mycelia presumably function through both biotic processes (microbial mineralization) and abiotic processes (disruption of stabilized mineral-proteinaceous complexes), whereas roots mainly function through biotic processes. Given that roots and mycelia are belowground symbionts, these two mechanisms are proposed to function together to promote N transformation and thus have significant ecological ramifications for N cycling in karst ecosystems.
... Typical rocky desertification areas are generally distributed in arid and semiarid areas (Prvlie, 2016;Prvlie et al., 2019). Southwest China is one of the three major continuous rocky desertification areas in the world, which is one of the regions experiencing the most severe rocky desertification globally covering approximately 1.9 million km 2 (approximately 0.54 million km 2 of which lies on carbonate rocks) (Zhang et al., 2016;Pan et al., 2016;Ajaj et al., 2017;Brandt et al., 2018;Guo et al., 2020). In the Southwest Karst Mountain Region of China, experiences serious rocky desertification due to widely distributed carbonatite and dolomite (Guo et al., 2020). ...
Rocky desertification is a ubiquitous natural landscape in fragile karst areas, which has serious side effects on socioeconomic development and environmental protection. In order to explore in-depth the relationship between soil bacteria, plant communities and soil properties, species composition of herbs and shrubs was investigated, and soil properties were determined. Changes in soil bacterial community structure were detected by high-throughput sequencing of 16S rRNA V3-V4 regions. We found that the species compositions of herbs and shrubs was significantly different among the different rocky desertification grade. The soil bacterial phyla, Proteobacteria, Actinobacteria, Acidobacteria and Chloroflexi, were the most abundant species in the microbial community. Redundancy analysis showed that there were 5, 4, 3 and 3 kinds of soil bacterial phyla in the community and played a key role in the interactions between phytocommunity, soil properties and bacteria from the non-rocky desertification to the intense rocky desertification areas, respectively. The phytocommunity was significantly correlated with environmental factors (pH, Ca, soil enzymes and soil organic carbon). The relative abundance of Verrucomicrobium was low but was significantly correlated with soil properties. The MetaCyc pathway analysis found that the metabolic bacteria had the highest relative abundance in rocky desertification areas. The gradual reduction of the interactions of soil bacteria, plant community composition and multiple soil environmental factors resulted in the gradual degradation of rocky desertification. Our results provided a valuable scientific basis for understanding the interaction between soil bacteria, phytocommunity and soil properties in response to the evolution of rocky desertification, as well as highlighting the impact of microorganisms on different environmental factors.
... In seasonally dry systems, with increased denitrification in surface layers and leaching with high mean annual precipitation in tropical systems (Pataki et al., 2008;Craine et al., 2015;Roa-Fuentes et al., 2015;Campo, 2016), shallow soils may be expected to have available N with higher δ 15 N values. In addition, in karst soils, N can bind to organic matter in the presence of Ca from the calcium carbonate bedrock (Clarholm et al., 2015;Pan et al., 2016). This decreases plant available N, which may be exacerbated with increasing depth and decreasing soil within bedrock conduits from the surface. ...
Across the karst landscape of Quintana Roo, Mexico, plant access to nutrients and water appears limited by generally shallow soil. However, underlying this surface are heterogenous pockets in bedrock and deeper, stable groundwater, suggesting the potential for specialization by species in accessing soil resources. If species differentially access rock resources, divisions by functional groups may also be expected. In this study, shallow caves provided an opportunity to assess resource use strategies by direct, species-specific root observations coupled with traditional above ground measurements. Utilizing stable isotopes from stems and leaves (δ18O and δ13C), we investigated water access and water use efficiency of trees during the dry season to uncover relationships between rooting habit, tree size, and pre-determined functional groups based on leaf habit and wood density. Functional group membership did not predict measured stable isotope ratios, indicating that functional groups were poor predictors of resource use. We did find evidence for deep water use by select species and larger individuals. Interestingly, as trees became larger, δ13C increased to a threshold but then declined, suggesting increasing vulnerability to water limitation as trees increase in size, consistent with other seasonally dry tropical forests. Our work demonstrates that, although shallow soils likely drive strong resource limitations, co-occurring trees in karst ecosystems employ diverse resource acquisition strategies, suggesting important consequences for community composition and ecosystem function in the face of environmental change.
... Recent studies have suggested that plant roots and hyphae may play a crucial role in disrupting the stability of physicochemically protected SOM (Li et al. 2021;Pan et al. 2016; Thorley et al. 2014). Plant roots (and hyphae) release a vast portion of low-molecular-weight organic acids (LMWOAs) into the soil, which is a significant part of the water-soluble fractions of organic molecules in soils (Adeleke et al. 2017;Macias-Benitez et al. 2020). ...
... LMWOAs can complex with metals such as aluminum (Al) in soils, and the metal-complexing ability of organic acids is higher than those of amino acids, sugars, and phenolic acids (Hue et al. 1986). Besides, the delivery of LMWOAs can often accelerate native SOM mineralization in the rhizosphere (Pan et al. 2016) -which is known as the 'rhizosphere priming effect' (Dijkstra et al. 2013). Recent observations implied that this priming effect may be, to some extent, due to the ability of LMWOAs to disrupt SOM supramolecules, which causes the molecules to become vulnerable to microbial mineralization (Clarholm et al. 2015;Li et al. 2021). ...
... Previous efforts including laboratory experiments (Kong et al. 2014;Yuan et al. 2018), field observations (Gadd 1999;Pan et al. 2016;Strom et al. 2005), and model research (Clarholm et al. 2015;Lawrence et al. 2014), have been conducted to examine the influences of organic acids on the decomposition and dynamics of SOM. However, the majority of these studies have primarily examined the broad effects of organic acid input on the dynamics of SOM. ...
Purpose
Root-derived low-molecular-weight organic acids (LMWOAs) can impact the decomposition of soil organic matter (SOM) after being released into soils. However, the influence of individual LMWOA (e.g., oxalic acid) inputs on the destabilization of physicochemically protected SOM remains largely unknown.
Methods
Using artificial roots in a firmly controlled rhizosphere system, we daily added oxalic acid solutions to soils collected from two subalpine coniferous forests (a 70‐year‐old spruce plantation and a 200‐year‐old spruce‐fir dominated forest) and incubated the soils for over 25 days.
Results
The addition of oxalic acid significantly decreased the concentrations of iron bound in metal–organic complexes (Fe-MOCs), aluminum bound in metal–organic complexes (Al-MOCs), iron bound in short-range order phases (Fe-SROs), and iron bound in short-range order phases (Al-SROs) by 35%, 13%, 16%, and 30%, respectively, across the two forest soils. This result indicated that the oxalic acid addition promoted the destabilization of physicochemical-protected SOM. This destabilization of protected SOM was mainly caused by breaking crosslinking between carboxylic groups and multivalent cations and the release of aromatic carbon (C) from mineral-organic associations, as indicated by the concurrently decreased zeta potential and the prominently featured resonances assigned to aromatic functional groups in the corresponding spectra of the near edge X-ray absorption fine structure after the addition of oxalic acid. In addition, compared to that of the spruce plantation, the addition of oxalic acid induced greater changes in the metal pools (Fe and Al) bound in MOCs and SROs in the spruce-fir forest, which indicated that the oxalic acid-induced destabilization of physicochemical-protected SOM might also be regulated by native soil properties.
Conclusions
Our study demonstrates that the input of LMWOAs to soils could stimulate the destabilization of physicochemical-protected SOM, which is presumably involved in the disruption of mineral-organic associations by breaking the crosslinking bonds and releasing aromatic C. The destabilization of physicochemically protected SOM may accelerate SOM decomposition, and thus, the input of LMWOAs to soils has important ecological implications for the biogeochemical cycle in terrestrial ecosystems.
... Therefore, increasing the nutrient supply capacity for plants may be very important in this ecosystem. To tolerate the nutrientlimited stresses, plants have developed a wide variety of nutrient acquisition strategies, such as enhancing their symbiosis of roots with arbuscular mycorrhizal fungi and N-fixing bacteria [8,13,14], rhizosphere priming by exudations [15,16], and specific root length and root tips [17]. Moreover, fine root turnover is another effective strategy for plants responding to soil nutrient limitations [18]. ...
... In addition, a high fine root turnover rate is associated with a low lifespan [39,40], to maintain high nutrient absorption efficiency and cycling. In nutrient-limited soils, N and P nutrients would not sequestrate in fine roots but cycle quickly [16,42]. This might be consistent with the low N concentrations of fine roots in shrubland (Figure 3), due to N limitations in this vegetation. ...
Revealing the patterns of fine root turnover traits can aid our understanding of the mechanisms of fine roots in adapting to soil nutrient changes. In a karst ecosystem of southwest China, the fine root turnover rate, production, biomass, necromass, biomass/necromass ratio, as well as the soil total and available nitrogen (N) and phosphorus (P) concentrations, and root carbon (C) and N concentrations were analyzed in upper, middle, and lower slope positions of two vegetation types (shrubland and forest). The results showed that the soil total and available N and P and fine root production, biomass, and necromass were significantly higher in upper slope positions than those in lower slope positions in both vegetation types. However, the fine root turnover rates were slightly higher in upper positions than those in lower positions. In addition, fine root necromass was significantly lower in shrubland than that in forest, while the biomass/necromass ratio was the opposite. Therefore, fine root production and biomass were significantly affected by slope position, while the fine root biomass/necromass ratio was significantly influenced by vegetation type. Additionally, fine root necromass was significantly influenced by the slope position and vegetation, but the turnover rate was slightly impacted by the two factors. It was also found that fine root production, biomass, and necromass had significant positive correlations with the soil total and available N and P and root C concentrations, and had significant negative correlations with root N concentrations. Moreover, the biomass/necromass ratio was positively and negatively related to the root N concentrations and C/N ratios, respectively. Thus, the variations in these five parameters of fine root turnover were mainly explained by fine root nutrients and the interactive effects between fine root and soil nutrients. The above results indicated that these variations in fine roots responding to soil and root nutrient changes might be an adaptive mechanism to enhance plant nutrient acquisition in nutrient-poor karst ecosystems.
... Shrubs are widely distributed in the karst region of southwest China and are uniquely adapted for survival in conditions of drought, rocky establishments, and excessive calcium [12,13]. Accordingly, they have important applications for karst vegetation restoration [11,14]. ...
Plants associated with symbiotic nitrogen-fixers and soil free-living nitrogen-fixing bacteria are good indicators for detecting the source of nitrogen in natural ecosystems. However, the community composition and diversity of plants associated with symbiotic nitrogen-fixers and soil free-living nitrogen-fixing bacteria in karst shrub ecosystems remain poorly known. The community composition and diversity of soil free-living nitrogen-fixing bacteria and plants, as well as the soil physical–chemical properties were investigated in 21 shrub plots (including different topographies and plant types). The frequency of plants associated with symbiotic nitrogen-fixers was found to be low in the 21 shrub plots. The soil free-living nitrogen-fixing bacterial community structure varied among the 21 shrub soils. Based on a variance partitioning analysis, topography, plant type, and soil pH explained 48.5% of the observed variation in bacterial community structure. Plant type had a predominant effect on community structure, and topography (aspect and ascent) and soil pH had minor effects. A negative correlation between the abundance of the soil free-living nitrogen-fixing bacterial community and the richness index for plants associated with symbiotic nitrogen-fixers was observed. The result of the low frequency of plants associated with symbiotic nitrogen-fixers highlights the importance of sources of fixed nitrogen by soil free-living nitrogen-fixing bacteria in the nitrogen limitation shrub ecosystem of the karst regions.
... ( Table 2) were observed in our study, suggesting a greater demand by soil microorganisms for N and more severe N limitation in karst regions than the global average. Lower soil N∶P can be explained by the following: a large proportion of N is stabilised by becoming directly bound to calcium minerals or to numerous calcium bridges in soil organic matter in karst soils (Pan et al., 2016), leading to low N availability. Moreover, major loss of nutrients can occur via the underground drainage networks resulting from the shallow soil cover and the highly developed epikarst system in karst regions (Zeng et al., 2018;Liu et al., 2020), which rapidly leach away any newly dissolved available N. Conversely, P is mainly supplied by the weathering of rock in the natural environment (Ren et al., 2017). ...
Knowledge about resource limitations faced by soil microorganisms is crucial for understanding ecosystem functions and processes. In recent decades, vegetation restoration has been carried out in the degraded karst areas, leading to the alteration in the status of microbial resource limitation (MRL). However, mechanisms underlying MRL in different karst ecosystems remain poorly understood. Here we investigated MRL based on the theory of soil extracellular enzyme stoichiometry. Soil carbon (C), nitrogen (N), and phosphorus (P) acquiring enzyme activity (glucosidase, cellobiohydrolase, leucine aminopeptidase, urease and alkaline phosphatase) per unit microbial biomass carbon (MBCE) and per unit soil organic carbon (SOCE) of four main vegetation types (natural community, NC; ecological forest, EF; abandoned cropland, AC and economic plantation, EP) at 0-20 cm depth were measured in the karst areas in southwestern China. Significantly higher MBCE levels were found in EP than the other three vegetation types (p < 0.05), with EF having significantly higher SOCE than NC (p < 0.05), suggesting the highest metabolic activity and soil organic carbon (SOC) utilisation efficiency in EP and EF, respectively. C- and N-specific enzyme activity (MBCE and SOCE) were strongly negatively correlated with microbial biomass and soil C, N contents (p < 0.05), suggesting microbial resource requirement promotes the production of specific enzyme in resource-deficient ecosystems. Homeostasis analysis of microbial biomass C: N and resources C:N for all communities showed no homeostasis, indicating the microorganisms may be auto-trophic to meet their N demands. In addition, the specific enzyme C:N ratios were less than 1, the N :P ratios were greater than 1, and vector angles were all less than 45 degrees in all four types of vegetation restoration, indicating clear N limitation. A homeostasis analysis, as well as extracellular enzymatic stoichiometry and vector analysis, all suggested that soil microorganisms in the four vegetation types were nitrogen-limited, with NC most severely affected. Overall, we suggest that nitrogenous fertilisers should be added to restore the balance of elements while recovering the karst ecosystems.
