Evaluation of Microbe-Driven Soil Organic Matter Quantity and Quality by Thermodynamic Theory

Microbial communities are known to be important drivers of organic matter (OM) accumulation in terrestrial ecosystems. However, despite the importance of these soil microbes and processes, the mechanisms behind these microbial-SOM associations remain poorly understood. ABSTRACT Microbial communities, coupled with substrate quality and availability, regulate the stock (formation versus mineralization) of soil organic matter (SOM) in terrestrial ecosystems. However, our understanding of how soil microbes interact with contrasting substrates influencing SOM quantity and quality is still very superficial. Here, we used thermodynamic theory principles and Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) to evaluate the linkages between dissolved organic matter (DOM [organic substrates in soil that are readily available]), thermodynamic quality, and microbial communities. We investigated soils from subtropical paddy ecosystems across a 1,000-km gradient and comprising contrasting levels of SOM content and nutrient availability. Our region-scale study suggested that soils with a larger abundance of readily accessible resources (i.e., lower Gibbs free energy) supported higher levels of microbial diversity and higher SOM content. We further advocated a novel phylotype-level microbial classification based on their associations with OM quantities and qualities and identified two contrasting clusters of bacterial taxa: phylotypes that are highly positively correlated with thermodynamically favorable DOM and larger SOM content versus those which are associated with less-favorable DOM and lower SOM content. Both groups are expected to play critical roles in regulating SOM contents in the soil. By identifying the associations between microbial phylotypes of different life strategies and OM qualities and quantities, our study indicates that thermodynamic theory can act as a proxy for the relationship between OM and soil microbial communities and should be considered in models of soil organic matter preservation. IMPORTANCE Microbial communities are known to be important drivers of organic matter (OM) accumulation in terrestrial ecosystems. However, despite the importance of these soil microbes and processes, the mechanisms behind these microbial-SOM associations remain poorly understood. Here, we used the principles of thermodynamic theory and novel Fourier transform ion cyclotron resonance mass spectrometry techniques to investigate the links between microbial communities and dissolved OM (DOM) thermodynamic quality in soils across a 1,000-km gradient and comprising contrasting nutrient and C contents. Our region-scale study provided evidence that soils with a larger amount of readily accessible resources (i.e., lower Gibbs free energy) supported higher levels of microbial diversity and larger SOM content. Moreover, we created a novel phylotype-level microbial classification based on the associations between microbial taxa and DOM quantities and qualities. We found two contrasting clusters of bacterial taxa based on their level of association with thermodynamically favorable DOM and SOM content. Our study advances our knowledge on the important links between microbial communities and SOM. Moreover, by identifying the associations between microbial phylotypes of different life strategies and OM qualities and quantities, our study indicates that thermodynamic theory can act as a proxy for the relationship between OM and soil microbial communities. Together, our findings support that the association between microbial species taxa and substrate thermodynamic quality constituted an important complement explanation for soil organic matter preservation.