A bacterial pioneer produces cellulase complexes that persist through community succession
Cultivation of microbial consortia provides low-complexity communities that can serve as tractable models to understand community dynamics. Time-resolved metagenomics demonstrated that an aerobic cellulolytic consortium cultivated from compost exhibited community dynamics consistent with the definition of an endogenous heterotrophic succession. The genome of the proposed pioneer population, ‘Candidatus Reconcilibacillus cellulovorans’, possessed a gene cluster containing multidomain glycoside hydrolases (GHs). Purification of the soluble cellulase activity from a 300litre cultivation of this consortium revealed that ~70% of the activity arose from the ‘Ca. Reconcilibacillus cellulovorans’ multidomain GHs assembled into cellulase complexes through glycosylation. These remarkably stable complexes have supramolecular structures for enzymatic cellulose hydrolysis that are distinct from cellulosomes. The persistence of these complexes during cultivation indicates that they may be active through multiple cultivations of this consortium and act as public goods that sustain the community. The provision of extracellular GHs as public goods may influence microbial community dynamics in native biomass-deconstructing communities relevant to agriculture, human health and biotechnology.
Plant polysaccharide hydrolysis is a critical process in the human microbiome۱, soil microbiomes۲ and microbiomes related to bioenergy production۳,۴,۵. Identifying glycoside hydrolases (GHs) responsible for polysaccharide hydrolysis in these ecosystems has important implications for improving human health, managing agriculture and implementing biotechnological advances. Characterizing GHs from uncultivated organisms may also expand the diversity of protein structures that hydrolyse polysaccharides۶. However, these communities harbour substantial diversity, complicating the assignment of specific enzymatic roles to individual community members.
Model microbial consortia with simplified community compositions relative to native consortia have been identified as important systems to develop a mechanistic understanding of community function۷. Methods to cultivate these model consortia include combining isolates from native consortia and adapting native communities through selective pressure۸. These model consortia have enabled the assignment of function to specific microbial community members, clarified successional structures in communities۹ and identified previously unknown protein functions۱۰. Cultivation of model consortia that hydrolyse cellulose, the most abundant plant polysaccharide۱۱, has produced low-complexity communities where cellulose hydrolysis can be assigned to specific populations and linked to community structure and dynamics۱۲,۱۳.
Here, we report that a model cellulolytic consortium derived from compost was reproducibly cultivated aerobically at 15 l and 300 l. The proposed pioneer population۷ in this community, present at ~1% abundance at the time of culture harvest, produced multidomain cellulases that persisted through microbial succession and were the most active cellulases in the culture. These cellulases were organized in protein complexes that are distinct from cellulosomes۸ isolated from anaerobic bacteria. The persistence of these unusually stable complexes indicates that they may act as public goods۱۴ that sustain the community.
