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Interactions between microbial diversity and substrate chemistry determine the fate of carbon in soil.

ABSTRACT: Microbial decomposition drives the transformation of plant-derived substrates into microbial products that form stable soil organic matter (SOM). Recent theories have posited that decomposition depends on an interaction between SOM chemistry with microbial diversity and resulting function (e.g., enzymatic capabilities, growth rates). Here, we explicitly test these theories by coupling quantitative stable isotope probing and metabolomics to track the fate of ¹³C enriched substrates that vary in chemical composition as they are assimilated by microbes and transformed into new metabolic products in soil. We found that differences in forest nutrient economies (e.g., nutrient cycling, microbial competition) led to arbuscular mycorrhizal (AM) soils harboring greater diversity of fungi and bacteria than ectomycorrhizal (ECM) soils. When incubated with ¹³C enriched substrates, substrate type drove shifts in which species were active decomposers and the abundance of metabolic products that were reduced or saturated in the highly diverse AM soils. The decomposition pathways were more static in the less diverse, ECM soil. Importantly, the majority of these shifts were driven by taxa only present in the AM soil suggesting a strong link between microbial identity and their ability to decompose and assimilate substrates. Collectively, these results highlight an important interaction between ecosystem-level processes and microbial diversity; whereby the identity and function of active decomposers impacts the composition of decomposition products that can form stable SOM.

SUBMITTER: Raczka NC

PROVIDER: S-EPMC8481224 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Interactions between microbial diversity and substrate chemistry determine the fate of carbon in soil.

Raczka Nanette C NC Piñeiro Juan J Tfaily Malak M MM Chu Rosalie K RK Lipton Mary S MS Pasa-Tolic Ljiljana L Morrissey Ember E Brzostek Edward E

Scientific reports 20210929 1

Microbial decomposition drives the transformation of plant-derived substrates into microbial products that form stable soil organic matter (SOM). Recent theories have posited that decomposition depends on an interaction between SOM chemistry with microbial diversity and resulting function (e.g., enzymatic capabilities, growth rates). Here, we explicitly test these theories by coupling quantitative stable isotope probing and metabolomics to track the fate of <sup>13</sup>C enriched substrates tha ...[more]

PMID: 34588474

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Project description:Mathematical models do not explicitly represent the influence of soil microbial diversity on soil organic carbon (SOC) dynamics despite recent evidence of relationships between them. The objective of the present study was to statistically investigate relationships between bacterial and fungal diversity indexes (richness, evenness, Shannon index, inverse Simpson index) and decomposition of different pools of soil organic carbon by measuring dynamics of CO2 emissions under controlled conditions. To this end, 20 soils from two different land uses (cropland and grassland) were incubated with or without incorporation of 13C-labelled wheat-straw residue. 13C-labelling allowed us to study residue mineralisation, basal respiration and the priming effect independently. An innovative data-mining approach was applied, based on generalized additive models and a predictive criterion. Results showed that microbial diversity indexes can be good covariates to integrate in SOC dynamics models, depending on the C source and the processes considered (native soil organic carbon vs. fresh wheat residue). Specifically, microbial diversity indexes were good candidates to help explain mineralisation of native soil organic carbon, while priming effect processes seemed to be explained much more by microbial composition, and no microbial diversity indexes were found associated with residue mineralisation. Investigation of relationships between diversity and mineralisation showed that higher diversity, as measured by the microbial diversity indexes, seemed to be related to decreased CO2 emissions in the control soil. We suggest that this relationship can be explained by an increase in carbon yield assimilation as microbial diversity increases. Thus, the parameter for carbon yield assimilation in mathematical models could be calculated as a function of microbial diversity indexes. Nonetheless, given limitations of the methods used, these observations should be considered with caution and confirmed with more experimental studies. Overall, along with other studies on relationships between microbial community composition and SOM dynamics, this study suggests that overall measures of microbial diversity may constitute relevant ways to include microbial diversity in models of SOM dynamics.

Project description:In subtropical forest ecosystems with few phosphorus (P) inputs, P availability and forest productivity depend on soil organic P (Po) mineralization. However, the mechanisms by which the microbial community determines the status and fate of soil Po mineralization remain unclear. In the present study, soils were collected from three typical forest types: secondary natural forest (SNF), mixed planting, and monoculture forest of Chinese fir. The P fractions, Po-mineralization ability, and microbial community in the soils of different forest types were characterized. In addition, we defined Po-mineralizing taxa with the potential to interact with the soil microbial community to regulate Po mineralization. We found that a higher labile P content persisted in SNF and was positively associated with the Po-mineralization capacity of the soil microbial community. In vitro cultures of soil suspensions revealed that soil Po mineralization of three forest types was distinguished by differences in the composition of fungal communities. We further identified broad phylogenetic lineages of Po-mineralizing fungi with a high intensity of positive interactions with the soil microbial community, implying that the facilitation of Po-mineralizing taxa is crucial for soil P availability. Our dilution experiments to weaken microbial interactions revealed that in SNF soil, which had the highest interaction intensity of Po-mineralizing taxa with the community, Po-mineralization capacity was irreversibly lost after dilution, highlighting the importance of microbial diversity protection in forest soils. In summary, this study demonstrates that the interactions of Po-mineralizing microorganisms with the soil microbial community are critical for P availability in subtropical forests.IMPORTANCEIn subtropical forest ecosystems with few phosphorus inputs, phosphorus availability and forest productivity depend on soil organic phosphorus mineralization. However, the mechanisms by which the microbial community interactions determine the mineralization of soil organic phosphorus remain unclear. In the present study, soils were collected from three typical forest types: secondary natural forest, mixed planting, and monoculture forest of Chinese fir. We found that a higher soil labile phosphorus content was positively associated with the organic phosphorus mineralization capacity of the soil microbial community. Soil organic phosphorus mineralization of three forest types was distinguished by the differences in the composition of fungal communities. The positive interactions between organic phosphorus-mineralizing fungi and the rest of the soil microbial community facilitated organic phosphorus mineralization. This study highlights the importance of microbial diversity protection in forest soils and reveals the microbial mechanism of phosphorus availability maintenance in subtropical forest ecosystems.

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Interactions between microbial diversity and substrate chemistry determine the fate of carbon in soil.

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Interactions between microbial diversity and substrate chemistry determine the fate of carbon in soil.

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