Shifts in microbial metabolic pathway for soil carbon accumulation along subtropical forest succession

Abstract

The dynamic process of forest succession is important for terrestrial ecosystems where soil organic matter (SOM) primarily controls biogeochemical cycles and is driven by soil microorganisms. Carbon (C) incorporation into SOM occurs along two different microbial metabolic pathways: ex vivo mostly extracellular enzymatic modification and in vivo turnover within the cells, highlighting the importance of microbial catabolism and anabolism respectively during soil C transformation and sequestration. However, identifying the dual C pathways and understanding the microbially-mediated SOM transformation during forest succession remains elusive, particularly with respect to interactions in the rhizosphere. Here, we used a series of biomarkers, including amino sugars, phospholipid fatty acids, and neutral sugars, to explore how forest succession and rhizosphere dynamics affect microbial contribution to soil organic carbon (SOC) in three successional stages of a subtropical forest ecosystem. We observed generally consistent increases in amino sugar and SOC with forest age in both bulk and rhizosphere soil, demonstrating that microorganisms facilitate SOC accumulation through the in vivo pathway along the successional gradient. The ratio of amino sugar-C to SOC (AS-C/SOC) exhibited a greater increase in bulk than in rhizosphere soil along the successional gradient, indicating the microbial in vivo pathway was relatively more important for SOC accumulation in bulk than in rhizosphere soil. Given there was a significant decrease in the ratios of hexose-to-pentose sugars [(galactose + mannose)/(arabinose + xylose), indicating the contribution of sugars derived from microbes and plants to labile soil C], we hold the opinion that relatively limited microbial C processing occurred in the rhizosphere along the forest successional gradient. Therefore, the microbial ex vivo pathway where microorganisms decomposed (structurally modified) fine root litter that was incorporated into SOC was relatively more important in rhizosphere than in bulk soil for SOC variation during forest succession. Our findings emphasize the role of microbes transforming organic matter in both bulk and rhizosphere soil in a subtropical forest successional gradient and help to enhance our understanding of the function and ecosystem services of these environments.