Abstract
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.
Highlights
Cultivation of microbial consortia provides low-complexity communities that can serve as tractable models to understand community dynamics
This work has demonstrated that an aerobic cellulolytic microbial consortium derived from compost can be reproducibly cultivated and can be scaled to grow at 300 l
This community provides an excellent model with which to understand the community dynamics of cellulolytic consortia and uncover enzymes missed by analysis focused solely on culturable isolates
Summary
Cultivation of microbial consortia provides low-complexity communities that can serve as tractable models to understand community dynamics. 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. Cultivation of model consortia that hydrolyse cellulose, the most abundant plant polysaccharide[11], has produced low-complexity communities where cellulose hydrolysis can be assigned to specific populations and linked to community structure and dynamics[12,13]. The proposed pioneer population[7] 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 cellulosomes[8] isolated from anaerobic bacteria. The persistence of these unusually stable complexes indicates that they may act as public goods[14] that sustain the community
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