Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of agricultural soil

Abstract Background Microorganisms that degrade cellulose utilize extracellular processes that yield free intermediates which promote interactions with non-cellulolytic organisms. We hypothesized that these interactions determine the ecological and physiological traits governing the fate of cellulosic carbon (C) in soil. We employed metagenomic-SIP and metaproteomics to characterize the attributes of cellulolytic and non-cellulolytic microbes accessing 13C from cellulose. We hypothesized that cellulolytic taxa would exhibit competitive traits to limit access, while non-cellulolytic taxa would display metabolic dependency, such as signatures of adaptive gene loss. We tested this hypothesis by evaluating genomic traits indicative of competitive exclusion or metabolic dependency, such as antibiotic production, growth rate, surface attachment, biomass degrading potential and auxotrophy. Results The most 13C-enriched taxa were cellulolytic Cellvibrio (Gammaproteobacteria) and Chaetomium (Ascomycota), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. These ruderal taxa were common indicators of soil disturbance in agroecosystems, such as tillage and fertilization. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria, demonstrating differences in dependency among cellulose degraders. Non-cellulolytic taxa that accessed 13C from cellulose (Planctomycetales, Verrucomicrobia and Vampirovibrionales) were highly dependent, as indicated by patterns of auxotrophy and 13C-labeling (i.e. partial labelling or labeling at later-stages). Major 13C-labeled cellulolytic microbes (e.g. Sorangium, Actinomycetales, Rhizobiales and Caulobacteraceae) possessed adaptations for surface colonization (e.g. gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposition. Conclusions Our results demonstrate that access to cellulose was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion. These trade-offs influence microbial growth dynamics on particulate organic carbon and reveal that the fate of carbon is governed by a complex economy within the microbial community. We propose three ecological groups for microbes participating in this economy: (i) independent primary degraders, (ii) integrated primary degraders and (iii) mutualists, opportunists and parasites.