An adhesin from hydrogen‐utilizing rumen methanogen Methanobrevibacter ruminantium M1 binds a broad range of hydrogen‐producing microorganisms

Abstract

SummarySymbiotic associations are ubiquitous in the microbial world and have a major role in shaping the evolution of both partners. One of the most interesting mutualistic relationships exists between protozoa and methanogenic archaea in the fermentative forestomach (rumen) of ruminant animals. Methanogens reside within and on the surface of protozoa as symbionts, and interspecies hydrogen transfer is speculated to be the main driver for physical associations observed between the two groups. In silico analyses of several rumen methanogen genomes have previously shown that up to 5% of genes encode adhesin-like proteins, which may be central to rumen interspecies attachment. We hypothesized that adhesin-like proteins on methanogen cell surfaces facilitate attachment to protozoal hosts. Using phage display technology, we have identified a protein (Mru_1499) from Methanobrevibacter ruminantium M1 as an adhesin that binds to a broad range of rumen protozoa (including the genera Epidinium and Entodinium). This unique adhesin also binds the cell surface of the bacterium Butyrivibrio proteoclasticus, suggesting a broad adhesion spectrum for this protein.

The role of condensed tannins in ruminant animal production: advances, limitations and future directions

“…One of the many important symbiotic associations formed in the rumen is that of the relationship between methanogenic archaea and ciliated protozoa (Ng et al, 2016). It has been proposed that this association occurs to facilitate interspecies transfer of metabolic H 2 from protozoa to methanogens.…”

“…One hypothesis is that CT act directly upon methanogens in the rumen. Ng et al (2016) reported the existence of a protein-based adhesin probably located at the tips of fimbriae that function in facilitation of the methanogen-protozoa symbiosis. Parts of the cell envelope, including the cell membrane, wall, and glycocalyx, also contain protein.…”

The Draft Genome of the Non-Host-AssociatedMethanobrevibacter arboriphilusStrain DH1 Encodes a Large Repertoire of Adhesin-Like Proteins

“…This finding may indicate that at least some ALPs, if they function as adhesins, may have interaction partners other than host tissues. This hypothesis is corroborated by two findings: first, a recent analysis of a M. ruminantium ALP, Mru_1499, revealed that a domain of these adhesins may be important for the interaction between methanogens and protozoa and bacteria [8]. However, the large and diverse repertoire of methanogen ALPs encoded by some Methanobrevibacter genomes suggests that other interaction partners also need to be considered and that ALP subgroups/domains may have different host/target specificity.…”

“…Yet some species of this genus appear to be more indicative for certain environments than others. For example, previous studies have shown that the methanogen communities in the rumens of cattle and sheep are dominated by two different Methanobrevibacter species, M. gottschalkii and M. ruminantium [4, 5], while microbiota analyses of the human gut revealed that M. smithii is the predominant methanogen in this habitat [6–8]. The growing number of sequenced Methanobrevibacter genomes allows performing comparative genome analysis in order to identify traits in strains and species that have adapted to a specific environment.…”

“…This and the remote similarity of these proteins to bacterial homologues led to the annotation of these proteins as adhesin-like proteins (ALPs) [22]. The role for most ALPs remains speculative as there is only limited functional evidence that these proteins act as adhesins and what their targets could be [8]. However, their high abundance in host-associated methanogens suggests a potential role in methanogen-vertebrate host interaction.…”