Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins - PubMed (original) (raw)

. 2011 Mar 15;108 Suppl 1(Suppl 1):4599-606.

doi: 10.1073/pnas.1000071108. Epub 2011 Feb 11.

Catherine A Lozupone, Federico E Rey, Meng Wu, Janaki L Guruge, Aneesha Narra, Jonathan Goodfellow, Jesse R Zaneveld, Daniel T McDonald, Julia A Goodrich, Andrew C Heath, Rob Knight, Jeffrey I Gordon

Affiliations

Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins

Elizabeth E Hansen et al. Proc Natl Acad Sci U S A. 2011.

Abstract

The human gut microbiota harbors three main groups of H(2)-consuming microbes: methanogens including the dominant archaeon, Methanobrevibacter smithii, a polyphyletic group of acetogens, and sulfate-reducing bacteria. Defining their roles in the gut is important for understanding how hydrogen metabolism affects the efficiency of fermentation of dietary components. We quantified methanogens in fecal samples from 40 healthy adult female monozygotic (MZ) and 28 dizygotic (DZ) twin pairs, analyzed bacterial 16S rRNA datasets generated from their fecal samples to identify taxa that co-occur with methanogens, sequenced the genomes of 20 M. smithii strains isolated from families of MZ and DZ twins, and performed RNA-Seq of a subset of strains to identify their responses to varied formate concentrations. The concordance rate for methanogen carriage was significantly higher for MZ versus DZ twin pairs. Co-occurrence analysis revealed 22 bacterial species-level taxa positively correlated with methanogens: all but two were members of the Clostridiales, with several being, or related to, known hydrogen-producing and -consuming bacteria. The M. smithii pan-genome contains 987 genes conserved in all strains, and 1,860 variably represented genes. Strains from MZ and DZ twin pairs had a similar degree of shared genes and SNPs, and were significantly more similar than strains isolated from mothers or members of other families. The 101 adhesin-like proteins (ALPs) in the pan-genome (45 ± 6 per strain) exhibit strain-specific differences in expression and responsiveness to formate. We hypothesize that M. smithii strains use their different repertoires of ALPs to create diversity in their metabolic niches, by allowing them to establish syntrophic relationships with bacterial partners with differing metabolic capabilities and patterns of co-occurrence.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Correlation of methanogen levels in the fecal microbiota of MZ and DZ co-twins. The presence and levels of fecal methanogens were defined by qPCR assay that targeted the mcrA gene in samples obtained from MZ twin pairs (A) (n = 40) and DZ twin pairs (B) (n = 28). Dashed lines represent 95% confidence intervals for linear regression. (C) Correlation between mcrA levels in fecal samples collected at two time points per individual (2-mo interval between sampling). All axes in A_–_C are log10 (genome equivalents per ng total DNA +1).

Fig. 2.

Fig. 2.

Normalized RNA-Seq reads assigned to the gene encoding an ammonium transporter (AmtB) and ECs involved in ammonia assimilation. (A) Overview of the two pathways of M. smithii for assimilating ammonia: The energy-dependent glutamine synthetase-glutamate synthase pathway has high affinity for ammonia (red arrow); an ATP-independent pathway has lower affinity (orange). (B) Strain-specific differences in the relative expression of components of the high affinity Gln pathway and the energy-independent low affinity pathway for ammonia assimilation. Mean values ± SEM are plotted. Colors represent components of the two pathways shown in A; color codes are coordinated between A and B. (C) Strain-specific differences in levels of expression of amtB. P < 0.0001 by one-way ANOVA.

Fig. 3.

Fig. 3.

Differential expression of M. smithii adhesin-like proteins (ALPs). Members of selected ALP OGUs with strain-specific differences in their expression profiles (A) and strain-specific, as well as OGU-associated, differences in their sensitivity to levels of formate during midlog phase growth (B). OGUs 112, 412, 827, and 208 exhibit strain-specific differences in their expression irrespective of formate concentration (one-way ANOVA, P < 0.0001), whereas OGUs 226, 287, 18, 133, and 37 contain at least one representative that is significantly regulated by formate concentration. Mean values ± SEM are plotted (n = 6 replicates per condition). * indicates a ≥2-fold difference, PPDE ≥ 0.97 (

Dataset S1, Table S7

).

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