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A Closer Look at Bacteroides: Phylogenetic Relationship and Genomic Implications of a Life in the Human Gut

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Abstract

The human gut is extremely densely inhabited by bacteria mainly from two phyla, Bacteroidetes and Firmicutes, and there is a great interest in analyzing whole-genome sequences for these species because of their relation to human health and disease. Here, we do whole-genome comparison of 105 Bacteroidetes/Chlorobi genomes to elucidate their phylogenetic relationship and to gain insight into what is separating the gut living Bacteroides and Parabacteroides genera from other Bacteroidetes/Chlorobi species. A comprehensive analysis shows that Bacteroides species have a higher number of extracytoplasmic function σ factors (ECF σ factors) and two component systems for extracellular signal transduction compared to other Bacteroidetes/Chlorobi species. A whole-genome phylogenetic analysis shows a very little difference between the Parabacteroides and Bacteroides genera. Further analysis shows that Bacteroides and Parabacteroides species share a large common core of 1,085 protein families. Genome atlases illustrate that there are few and only small unique areas on the chromosomes of four Bacteroides/Parabacteroides genomes. Functional classification to clusters of othologus groups show that Bacteroides species are enriched in carbohydrate transport and metabolism proteins. Classification of proteins in KEGG metabolic pathways gives a detailed view of the genome’s metabolic capabilities that can be linked to its habitat. Bacteroides pectinophilus and Bacteroides capillosus do not cluster together with other Bacteroides species, based on analysis of 16S rRNA sequence, whole-genome protein families and functional content, 16S rRNA sequences of the two species suggest that they belong to the Firmicutes phylum. We have presented a more detailed and precise description of the phylogenetic relationships of members of the Bacteroidetes/Chlorobi phylum by whole genome comparison. Gut living Bacteroides have an enriched set of glycan, vitamin, and cofactor enzymes important for diet digestion.

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Acknowledgements

We gratefully acknowledge the Knut and Alice Wallenberg Foundation and the Chalmers Foundation for financial support. We thank Dina Petranovic for helpful discussions for the manuscript.

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Authors and Affiliations

  1. Department of Chemical and Biological Engineering, Chalmers University of Technology, 412 96, Gothenburg, Sweden

    Fredrik H. Karlsson, Jens Nielsen & Intawat Nookaew

  2. Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800, Lyngby, Denmark

    David W. Ussery

Authors
  1. Fredrik H. Karlsson
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  2. David W. Ussery
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  3. Jens Nielsen
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  4. Intawat Nookaew
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Correspondence to Intawat Nookaew.

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Supplementary Table 1

Bacteroidetes/Chlorobi genomes in this study. (RTF 332 kb)

Supplementary Figure 1

Transmembrane helices, sigma factors and two-component systems were predicted with hidden Markov models (HMM) with an e value cutoff of 0.01 [17, 18, 20], signal peptides were identified with SignalP 3.0 [3]. In each genome, the total number of features were counted. Mann–Whitney U test was used to calculate the probability of an equal distribution between Bacteroides, Parabacteroides, and other genomes, comparisons are indicated by B, P, and O, respectively. tRNAs total number of tRNA genes, ecf ECF-sigma factors, HisKA_1 two-component histidine kinase 1, RRreciever two-component response regulator, Total total number of proteins, CYT cytosolic proteins, SpI proteins with signal peptidase I cleavage site, SpII proteins with signal peptidase II cleavage site, TMH proteins with at least one trans-membrane helix. (PDF 30 kb)

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Karlsson, F.H., Ussery, D.W., Nielsen, J. et al. A Closer Look at Bacteroides: Phylogenetic Relationship and Genomic Implications of a Life in the Human Gut. Microb Ecol 61, 473–485 (2011). https://doi.org/10.1007/s00248-010-9796-1

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