The Coupled Nature of DOM: Combining Microbial and Molecular Perspectives on Plant Litter Decomposition

During the decomposition of senescent plant material in the litter layer, microorganisms majorly control the formation, decomposition and transformation of dissolved organic matter (DOM). There is growing recognition that metabolic processing of DOM can shape both the molecular composition as well as the microbial community structure in a highly interconnected manner. To elucidate the coupled nature of DOM evolution, we performed plant litter decomposition experiments using senescent beech and oak leaves, pine needles and grasses. We combined the results of 120 non-targeted ultrahigh resolution mass spectra in a weighted correlation network analysis. The produced network resumed the combination of all decomposition series and consisted of ten distinct subnetworks that reflected the individual litter inputs as well as their temporal evolution. We further assigned chemical structure and metabolic pathway suggestions to sum formulae from the KEGG database and were able to identify distinct metabolic phases during the decomposition process. An initial phase was characterized by the release of plant phenylpropanoids and lignin-derivatives, followed by a temporary increase of compounds with antibiotic potential. Our data suggested a shift from the initial colonization of the plant material and decomposition of lignin to competitive secondary metabolism. To identify the role of microorganism-specific metabolic strategies, we connected 16S rRNA gene analyses to DOM evolution using genome-scale models of microbial metabolism. We found that the initial metabolization of lignin-derivatives was likely driven by specific microorganism-DOM interactions. In contrast, the following competitive secondary metabolism resulted in more unspecific microbial metabolites being present in DOM. By combining molecular and microbial perspectives with novel data processing approaches and database integration, our study highlights specific and unspecific microorganism-DOM interactions during plant litter decomposition. We emphasize the need for a better understanding of DOM as part of a complex metabolic network and advocate for the adaptation of freely available bioinformatics tools for the elucidation of the co-evolution of DOM and microbial communities.