Abstract
BackgroundIn nature, obligate herbivorous ruminants have a close symbiotic relationship with their gastrointestinal microbiome, which proficiently deconstructs plant biomass. Despite decades of research, lignocellulose degradation in the rumen has thus far been attributed to a limited number of culturable microorganisms. Here, we combine meta-omics and enzymology to identify and describe a novel Bacteroidetes family (“Candidatus MH11”) composed entirely of uncultivated strains that are predominant in ruminants and only distantly related to previously characterized taxa.ResultsThe first metabolic reconstruction of Ca. MH11-affiliated genome bins, with a particular focus on the provisionally named “Candidatus Paraporphyromonas polyenzymogenes”, illustrated their capacity to degrade various lignocellulosic substrates via comprehensive inventories of singular and multi-modular carbohydrate active enzymes (CAZymes). Closer examination revealed an absence of archetypical polysaccharide utilization loci found in human gut microbiota. Instead, we identified many multi-modular CAZymes putatively secreted via the Bacteroidetes-specific type IX secretion system (T9SS). This included cellulases with two or more catalytic domains, which are modular arrangements that are unique to Bacteroidetes species studied to date. Core metabolic proteins from Ca. P. polyenzymogenes were detected in metaproteomic data and were enriched in rumen-incubated plant biomass, indicating that active saccharification and fermentation of complex carbohydrates could be assigned to members of this novel family. Biochemical analysis of selected Ca. P. polyenzymogenes CAZymes further iterated the cellulolytic activity of this hitherto uncultured bacterium towards linear polymers, such as amorphous and crystalline cellulose as well as mixed linkage β-glucans.ConclusionWe propose that Ca. P. polyenzymogene genotypes and other Ca. MH11 members actively degrade plant biomass in the rumen of cows, sheep and most likely other ruminants, utilizing singular and multi-domain catalytic CAZymes secreted through the T9SS. The discovery of a prominent role of multi-modular cellulases in the Gram-negative Bacteroidetes, together with similar findings for Gram-positive cellulosomal bacteria (Ruminococcus flavefaciens) and anaerobic fungi (Orpinomyces sp.), suggests that complex enzymes are essential and have evolved within all major cellulolytic dominions inherent to the rumen.
Highlights
In nature, obligate herbivorous ruminants have a close symbiotic relationship with their gastrointestinal microbiome, which proficiently deconstructs plant biomass
MH11 and identify “Candidatus Paraporphyromonas polyenzymogenes” In order to resolve the taxonomy of AGa, we performed phylogenetic analyses using concatenated alignments of 16 single-copy ribosomal proteins (Fig. 1)
Our analysis indicated that AGa falls within a monophyletic family composed of six sheep rumen associated Uncultured Bacteria and Archaea (UBA) genomes within the order Bacteroidales in the Bacteroidetes phylum (Fig. 1)
Summary
Obligate herbivorous ruminants have a close symbiotic relationship with their gastrointestinal microbiome, which proficiently deconstructs plant biomass. Lignocellulose degradation in the rumen has far been attributed to a limited number of culturable microorganisms. Despite significant efforts over many decades, rumen cellulose degradation has so far been attributed to a limited number of culturable representatives, including Firmicutes and Fibrobacteres species. Fibrobacter succinogenes in turn uses an enigmatic mechanism that does not involve cellulosomes or known exocellulases implicated in secreted cellulase systems [3]. An aerobic soil Bacteroidete, Cytophaga hutchinsonii, has been suggested to use a non-classical cellulolytic mechanism during which the organism adheres closely to cellulose and glides across the substrate, degrading it with periplasmic and extracellular endocellulases that are secreted by the type IX secretion system (T9SS) [8]
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