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Evidence for plasmid-mediated salt tolerance in the human gut microbiome and potential mechanisms.

ABSTRACT: The human gut microbiome is critical to health and wellbeing. It hosts a complex ecosystem comprising a multitude of bacterial species, which contributes functionality that would otherwise be absent from the host. Transient and commensal bacteria in the gut must withstand many stresses. The influence of mobile genetic elements such as plasmids in stress adaptation within the ecosystem is poorly understood. Using a mobilomic approach we found evidence for plasmid-mediated osmotolerance as a phenotype amongst the Proteobacteria in healthy faecal slurries. A transconjugant carrying multiple plasmids acquired from healthy faecal slurry demonstrated increased osmotolerance in the presence of metal salts, particularly potassium chloride, which was not evident in the recipient. Pyrosequencing and analysis of the total plasmid DNA demonstrated the presence of plasmid-borne osmotolerance systems (including KdpD and H-NS) which may be linked to the observed phenotype. This is the first report of a transferable osmotolerance phenotype in gut commensals and may have implications for the transfer of osmotolerance in other niches.

SUBMITTER: Broaders E

PROVIDER: S-EPMC5831011 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Evidence for plasmid-mediated salt tolerance in the human gut microbiome and potential mechanisms.

Broaders Eileen E O'Brien Ciarán C Gahan Cormac G M CG Marchesi Julian R JR

FEMS microbiology ecology 20160204 3

The human gut microbiome is critical to health and wellbeing. It hosts a complex ecosystem comprising a multitude of bacterial species, which contributes functionality that would otherwise be absent from the host. Transient and commensal bacteria in the gut must withstand many stresses. The influence of mobile genetic elements such as plasmids in stress adaptation within the ecosystem is poorly understood. Using a mobilomic approach we found evidence for plasmid-mediated osmotolerance as a pheno ...[more]

PMID: 26850157

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Project description:Little is known regarding the pool of mobile genetic elements associated with the human gut microbiome. In this study we employed the culture independent TRACA system to isolate novel plasmids from the human gut microbiota, and a comparative metagenomic analysis to investigate the distribution and relative abundance of functions encoded by these plasmids in the human gut microbiome.Novel plasmids were acquired from the human gut microbiome, and homologous nucleotide sequences with high identity (>90%) to two plasmids (pTRACA10 and pTRACA22) were identified in the multiple human gut microbiomes analysed here. However, no homologous nucleotide sequences to these plasmids were identified in the murine gut or environmental metagenomes. Functions encoded by the plasmids pTRACA10 and pTRACA22 were found to be more prevalent in the human gut microbiome when compared to microbial communities from other environments. Among the most prevalent functions identified was a putative RelBE toxin-antitoxin (TA) addiction module, and subsequent analysis revealed that this was most closely related to putative TA modules from gut associated bacteria belonging to the Firmicutes. A broad phylogenetic distribution of RelE toxin genes was observed in gut associated bacterial species (Firmicutes, Bacteroidetes, Actinobacteria and Proteobacteria), but no RelE homologues were identified in gut associated archaeal species. We also provide indirect evidence for the horizontal transfer of these genes between bacterial species belonging to disparate phylogenetic divisions, namely Gram negative Proteobacteria and Gram positive species from the Firmicutes division.The application of a culture independent system to capture novel plasmids from the human gut mobile metagenome, coupled with subsequent comparative metagenomic analysis, highlighted the unexpected prevalence of plasmid encoded functions in the gut microbial ecosystem. In particular the increased relative abundance and broad phylogenetic distribution was identified for a putative RelBE toxin/antitoxin addiction module, a putative phosphohydrolase/phosphoesterase, and an ORF of unknown function. Our analysis also indicates that some plasmids or plasmid families are present in the gut microbiomes of geographically isolated human hosts with a broad global distribution (America, Japan and Europe), and are potentially unique to the human gut microbiome. Further investigation of the plasmid population associated with the human gut is likely to provide important insights into the development, functioning and evolution of the human gut microbiota.

Project description:Interest toward the human microbiome, particularly gut microbiome has flourished in recent decades owing to the rapidly advancing sequence-based screening and humanized gnotobiotic model in interrogating the dynamic operations of commensal microbiota. Although this field is still at a very preliminary stage, whereby the functional properties of the complex gut microbiome remain less understood, several promising findings have been documented and exhibit great potential toward revolutionizing disease etiology and medical treatments. In this review, the interactions between gut microbiota and the host have been focused on, to provide an overview of the role of gut microbiota and their unique metabolites in conferring host protection against invading pathogen, regulation of diverse host physiological functions including metabolism, development and homeostasis of immunity and the nervous system. We elaborate on how gut microbial imbalance (dysbiosis) may lead to dysfunction of host machineries, thereby contributing to pathogenesis and/or progression toward a broad spectrum of diseases. Some of the most notable diseases namely Clostridium difficile infection (infectious disease), inflammatory bowel disease (intestinal immune-mediated disease), celiac disease (multisystemic autoimmune disorder), obesity (metabolic disease), colorectal cancer, and autism spectrum disorder (neuropsychiatric disorder) have been discussed and delineated along with recent findings. Novel therapies derived from microbiome studies such as fecal microbiota transplantation, probiotic and prebiotics to target associated diseases have been reviewed to introduce the idea of how certain disease symptoms can be ameliorated through dysbiosis correction, thus revealing a new scientific approach toward disease treatment. Toward the end of this review, several research gaps and limitations have been described along with suggested future studies to overcome the current research lacunae. Despite the ongoing debate on whether gut microbiome plays a role in the above-mentioned diseases, we have in this review, gathered evidence showing a potentially far more complex link beyond the unidirectional cause-and-effect relationship between them.

Dataset Information

Evidence for plasmid-mediated salt tolerance in the human gut microbiome and potential mechanisms.

Publications

Evidence for plasmid-mediated salt tolerance in the human gut microbiome and potential mechanisms.

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