Human gut microbiome adopts an alternative state following small bowel transplantation

Abstract

Small bowel transplants provide an exceptional opportunity for long-term study of the microbial ecology of the human small bowel. The ileostomy created at time of transplant for ongoing monitoring of the allograft provides access to samples of ileal effluent and mucosal biopsies. In this study, we used qPCR to assay the bacterial population of the small bowel lumen of 17 small bowel transplant patients over time. Surprisingly, the posttransplant microbial community was found to be dominated by Lactobacilli and Enterobacteria, both typically facultative anaerobes. This represents an inversion of the normal community that is dominated instead by the strictly anaerobic Bacteroides and Clostridia. We found this inverted community also in patients with ileostomies who did not receive a transplant, suggesting that the ileostomy itself is the primary ecological determinant shaping the microbiota. After surgical closure of the ileostomy, the community reverted to the normal structure. Therefore, we hypothesized that the ileostomy allows oxygen into the otherwise anaerobic distal ileum, thus driving the transition from one microbial community structure to another. Supporting this hypothesis, metabolomic profiling of both communities demonstrated an enrichment for metabolites associated with aerobic respiration in samples from patients with open ileostomies. Viewed from an ecological perspective, the two communities constitute alternative stable states of the human ileum. That the small bowel appears to function normally despite these dramatic shifts suggests that its ecological resilience is greater than previously realized.16S ribosomal RNA ͉ alternative stable state ͉ human microbiota ͉ lactobacilli ͉ intestinal allograft

The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates

“…However, we observed a large proportion of anaerobes from the Clostridium cluster XIVa in our effluent samples, such as Coprococcus eutactus and relatives, which was detected up to 6% of the total community. Therefore, our data do not confirm a recent study that concluded oxygen exposure to have a major impact at the end of the terminal ileum in ileostomy patients (Hartman et al, 2009). Although we cannot fully exclude a potential role of oxygen, we consider it more likely that the absence of a colonic reflux explains our observations.…”

“…146 Mb of sequence information could be assembled into contigs that collectively encompass 63 Mb, with the largest contig being 78 kb, and leaving only 13% of the sequence-reads unassembled. This assembled proportion of sequences is considerably higher than previously observed with fecal metagenomes (Gill et al, 2006;Kurokawa et al, 2007), indicating a lower species diversity in the small intestine as compared with the colon, which is in line with the previous observations based on 16S rRNA genes (Hartman et al, 2009;Booijink et al, 2010). More than 170 000 genes could be assigned in the assembled contigs, of which 16% was complete.…”

“…In general, ileostomists that recover within months following the operation, can be considered healthy and enjoy an active life. A recent study suggested that oxygen might penetrate the small intestine via the stoma, resulting in increased facultative anaerobe populations (Hartman et al, 2009), but other studies have clearly established the significant abundance of typical strict anaerobes in effluent samples (Booijink et al, 2010).…”

Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups

“…Although phylogenetic coherence has previously been demonstrated for habitat preference at the class level (48,49) and genome size at the order level (50), we show that there are phylogenetically coherent pulse-response niches among cohabiting microorganisms. The high degree of phylogenetic coherence may reflect the complexity of survival of and resuscitation from desiccation.…”

Numerical ecology validates a biogeographical distribution and gender-based effect on mucosa-associated bacteria along the human colon

“…There is also one report of there being differences in mucosal oxygen concentration along the human colon, especially between the caecum and distal regions (pO 2 [mm Hg] being 33.7 ± 7.5 in the caecum, compared with 40.7 ± 8.2, 41.2 ± 8.7 and 39.7 ± 7.3 for the transverse colon, sigmoid colon and rectum, respectively (Sheridan et al, 1987)). Interestingly, recent studies linking a higher abundance of aerotolerant bacteria with ileal CD (Baumgart et al, 2007) and surgical intervention (Hartman et al, 2009) suggest that perturbations in oxygen concentration may be associated with the observed dysbiosis. Our findings are not inconsistent with these reports, and collectively, all three studies support the hypothesis that the dysbiosis seen with some types of IBD might initially be in response to the altered oxygenation state of the inflamed tissue.…”