Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon

Abstract

Hydrogenotrophic microbiota have a significant impact on colonic health; however, little is known about their diversity and ecology in situ. Here, molecular-based methods and multivariate analyses were used to examine the abundance and diversity of mucosa-associated hydrogenotrophic microbes in 90 biopsies collected from right colon, left colon and rectum of 25 healthy subjects. Functional genes of all three hydrogenotrophic groups were detected in at least one colonic region of all subjects. Methanogenic archaea (MA) constituted approximately one half of the hydrogenotrophic microbiota in each colonic region. Sulfate-reducing bacteria (SRB) were more abundant than acetogens in right colon, while acetogens were more abundant than SRB in left colon and rectum. MA genotypes exhibited low diversity, whereas SRB genotypes were diverse and generally similar across the three regions within subject but significantly variable among subjects. Multivariate cluster analysis defined subject-specific patterns for the diversity of SRB genotypes; however, neither subject-nor region-specific clusters were observed for the abundance of hydrogenotrophic functional genes. Sequence analyses of functional gene clones revealed that mucosa-associated SRB were phylogenetically related to Desulfovibrio piger, Desulfovibrio desulfuricans and Bilophila wadsworthia; whereas MA were related to Methanobrevibacter spp., Mb. smithii and the order Methanomicrobiales. Together these data demonstrate for the first time that the human colonic mucosa is persistently colonized by all three groups of hydrogenotrophic microbes, which exhibit segmental and interindividual variation in abundance and diversity.

H2metabolism is widespread and diverse among human colonic microbes

“…It is probable that the best-characterized pathways of colonic H 2 reoxidation, namely methanogenesis, sulfate-reduction, and potentially acetogenesis, 4,12,14,39 serve as only fractional sinks in the colonic H 2 budget. These processes have a major influence on the chemical composition of the human colon and its flatus, 4,12 enhance the diversity of gut microbiota, 3 and, particularly in the case of sulfate-reducers, have been extensively linked to human health and disease.…”

“…Secondly, fecal samples do not fully reflect the heterogeneity of the human colon over space and time. 12 Biopsy studies are likely to reveal more about the diversity and distribution of H 2 cycling, including why methanogens and sulfate-reducers are present and active in the human colon despite being outnumbered. 12 As reflected by our findings on the demography of colonic methanogenesis, 47 there is also need for clinical studies to explore how hydrogenase abundance and activity varies with factors such as subject weight, gender, race, and disease states.…”

“…11 There are at least 3 major pathways for disposal of the H 2 produced, namely methanogenesis, sulfate reduction, and acetogenesis. 12 The dominance of these pathways appears to vary among subjects, possibly as a result of competitive hydrogenotrophy. [13][14][15] However, there are also many reports of methanogens and sulfate-reducers co-existing in the colon.…”

“…[13][14][15] However, there are also many reports of methanogens and sulfate-reducers co-existing in the colon. 12,16,17 We have hypothesized that this is due to the large spatial and temporal variations in the chemical composition of the human colon, which would enable the formation of specific microhabitats dominated by different types of hydrogenotrophs. 4 Interspecies hydrogen transfer has been proposed to occur in the hydrogen-rich human colon, though microenvironmental niches in this mucosal ecosystem have not been studied and both the cellular and genetic bases for H 2 cycling are underexplored.…”

Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

“…Quantitative real-time PCR (qRT-PCR) was performed on a single sample from each individual using the SYBR Green PCR Master Mix (Applied Biosystems, Foster City, CA, USA) as described previously (Nava et al, 2012). Primers ACSF1/ ACSR1 (Gagen et al, 2010) and FTHFSf/FTHFSr (Leaphart and Lovell, 2001) targeting functional genes acs (acetyl-CoA synthase involved in the acetyl-CoA pathway) of acetogens were used.…”