The microbial decomposition of plant biomass is a major pathway for the release of carbon dioxide into the atmosphere, a critical step in the global carbon cycle. Few microbes possess the full suite of enzymes necessary to degrade plant biomass, and these organisms are often found within diverse communities in soil, leaf litter, and the guts of herbivores. Diversity-function relationships and microbe-microbe interactions are undoubtedly important for shaping these communities and their ability to degrade plant biomass. However, the complexity of natural environments hinders a clear identification of the interplay between community diversity and plant biomass decomposition or an understanding of the role of microbial interactions in this process. Here, we aimed to overcome this challenge by simplifying communities while preserving key microbe-microbe interactions using long-term serial enrichments in a minimal medium with cellulose, the dominant polymer within the plant cell wall, as the sole source of carbon and energy. Specifically, we inoculated cultures with material from leaf-cutter ant refuse dumps, a cellulose-rich reservoir responsible for considerable plant breakdown in Neotropical environments, and enriched microbial communities for up to sixty transfers (> 1 year).
The cellulolytic ability of four of the six communities drastically increased within five transfers then stabilized, while cellulolytic ability varied in the other two communities. Correspondingly, 16S rRNA gene sequencing showed that the “species” richness of each sample decreased and the community structure shifted for five passages then stabilized. The increase in cellulolytic ability correlated with an increase in abundance of known cellulose-degrading organisms Cellvibrio and Cellulomonas, while a diversity of taxa was maintained at low abundance. Over the course of one transfer, these cellulolytic organisms increased in relative abundance for the first 48 hours, until cellulose degradation was detected, and then non-cellulolytic community members increased in relative abundance. Metagenomic and metatranscriptomic analyses revealed that competition likely slowed cellulose degradation. Genes to metabolize cellulose breakdown products were highly expressed by a number of non-cellulolytic organisms in enrichment lines that were not efficient at breaking down cellulose, indicating competition for sugars slowed the rate of cellulose degradation. In addition, genes for localization and the production of antagonistic compounds were highly expressed across all communities. The results of this study demonstrate that not only general taxonomic diversity but also specific functional diversity and competition affect the stability and function of communities.