Abstract
Host glycans are paramount in regulating the symbiotic relationship between humans and their gut bacteria. The constant flux of host-secreted mucin at the mucosal layer creates a steady niche for bacterial colonization. Mucin degradation by keystone species subsequently shapes the microbial community. This study investigated the transcriptional response during mucin-driven trophic interaction between the specialised mucin-degrader Akkermansia muciniphila and a butyrogenic gut commensal Anaerostipes caccae. A. muciniphila monocultures and co-cultures with non-mucolytic A. caccae from the Lachnospiraceae family were grown anaerobically in minimal media supplemented with mucin. We analysed for growth, metabolites (HPLC analysis), microbial composition (quantitative reverse transcription PCR), and transcriptional response (RNA-seq). Mucin degradation by A. muciniphila supported the growth of A. caccae and concomitant butyrate production predominantly via the acetyl-CoA pathway. Differential expression analysis (DESeq 2) showed the presence of A. caccae induced changes in the A. muciniphila transcriptional response with increased expression of mucin degradation genes and reduced expression of ribosomal genes. Two putative operons that encode for uncharacterised proteins and an efflux system, and several two-component systems were also differentially regulated. This indicated A. muciniphila changed its transcriptional regulation in response to A. caccae. This study provides insight to understand the mucin-driven microbial ecology using metatranscriptomics. Our findings show that the expression of mucolytic enzymes by A. muciniphila increases upon the presence of a community member. This could indicate its role as a keystone species that supports the microbial community in the mucosal environment by increasing the availability of mucin sugars.
Highlights
The bacterial assembly at the mucosal layer of the human gastrointestinal tract is associated with gut health and disease (Ouwerkerk et al 2013; Tailford et al 2015)
This interplay leads to the formation of butyrate in the mucosal layer that is proposed to be beneficial to the host (Koh et al 2016; Louis and Flint 2017)
The majority of these mucin-degrading enzymes were predicted to function in the extracellular compartment (Ottman et al 2016), which could lead to the degradation of oligosaccharide chains consisting of GalNAc, GlcNAc, mannose, galactose, fucose and sialic acid (Moran et al 2011)
Summary
The bacterial assembly at the mucosal layer of the human gastrointestinal tract is associated with gut health and disease (Ouwerkerk et al 2013; Tailford et al 2015). The microbial composition of the healthy mucosa has not been properly defined, it has been observed that strong deviations in the mucosal microbiota are associated with inflammatory bowel disease (IBD) (Kostic et al 2014) and irritable bowel syndrome (IBS) (Lopez-Siles et al 2014). At this mucosal site, host-produced mucin glycans and bioactive compounds collectively exert a selective pressure that enriches for a sub-population of mucosaassociated bacteria (Koropatkin et al 2012; Ouwerkerk et al 2013; Schluter and Foster 2012). The potential therapeutic role of A. muciniphila has been demonstrated in mice by remedying symptoms of obesity and diabetes (Plovier et al 2017) as well as alcoholic liver disease (Grander et al 2017)
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