Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome

Abstract

The cellulosome is an extracellular multi-enzyme complex that is considered one of the most efficient plant cell wall-degrading strategies devised by nature. Its unique modular architecture, achieved by high affinity and specific interaction between protein modules (cohesins and dockerins) enables formation of various enzyme combinations. Extensive research has been dedicated to the mechanistic nature of the cellulosome complex. Nevertheless, little is known regarding its distribution and abundance among microbes in natural plant fibre-rich environments. Here, we explored these questions in bovine rumen microbial communities, specialized in efficient degradation of lignocellulosic plant material. We bioinformatically screened for cellulosomal modules in this complex environment using a previously published ultra-deep fibre-adherent rumen metagenome. Intriguingly, a large portion of the functions of the dockerin-containing proteins were related to alternative biological processes, and not necessarily to the classic fibre degradation function. Our analysis was experimentally validated by characterizing specific interactions between selected cohesins and dockerins and revealed that cellulosome is a more generalized strategy used by diverse bacteria, some of which were not previously associated with cellulosome production. Remarkably, our results provide additional proof of similarity among rumen microbial communities worldwide. This study suggests a broader and widespread role for the cellulosomal machinery in nature.

A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation

“…There were also several cases in which a single protein contained multiple dockerin domains, consistent with their function as adaptor proteins. The presence of dockerin domains in contigs from Bacteroidetes has been recently reported in both the bovine and the moose rumen metagenomes [ 39 , 57 ], implying that the ability to degrade cellulosome-based lignocellulose is a general feature of the rumen microbiome. However, recent evidence has also turned up dockerin domains in enzymes not known to be associated with fiber degradation [ 57 ].…”

Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system

“…Predicted peptidase modules were also found in scaffoldins ScaO and ScaP of B. cellulosolvens (associated with multiple PPC modules in addition to a single cohesin and dockerin), as well as in ScaO and ScaP of A. cellulolyticus [ 16 ]. The role of cellulosomal peptidases has not been defined experimentally, but recent studies have suggested the presence of peptidase modules associated with dockerins in the metagenome of the bovine rumen [ 50 ]. Similarly, in R. flavefaciens FD-1, numerous dockerins are associated with putative peptidase modules [ 33 ].…”

Comparative Metagenomics of Cellulose- and Poplar Hydrolysate-Degrading Microcosms from Gut Microflora of the Canadian Beaver (Castor canadensis) and North American Moose (Alces americanus) after Long-Term Enrichment

“…Similar to previous reports ( Finn et al, 2016 ), a few dockerin sequences were predicted to have appended DUF (i.e., DUF362, DUF1533, and DUF3237); however, the majority were not annotated as containing modules or domains functionally attributed to cellulosomes. In many cases, this could reflect sequence gaps due to incomplete metagenome assembly; however, it is also conceivable that dockerin–cohesin proteins might in fact participate in other biological functions, as suggested by a phylogenetically distinct group of cohesins discovered in the cow rumen metagenome ( Bensoussan et al, 2017 ).…”