Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome

Natasha K Dudek; Christine L Sun; David Burstein; Rose S Kantor; Daniela S Aliaga Goltsman; Elisabeth M Bik; Brian C Thomas; Jillian F Banfield; David A Relman

doi:10.1016/j.cub.2017.10.040

Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome

Curr Biol. 2017 Dec 18;27(24):3752-3762.e6. doi: 10.1016/j.cub.2017.10.040. Epub 2017 Nov 16.

Authors

Natasha K Dudek¹, Christine L Sun², David Burstein³, Rose S Kantor⁴, Daniela S Aliaga Goltsman², Elisabeth M Bik⁵, Brian C Thomas³, Jillian F Banfield⁶, David A Relman⁷

Affiliations

¹ Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.
² Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA; Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA.
³ Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA 94720, USA.
⁴ Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
⁵ Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA.
⁶ Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA 94720, USA; Earth and Environmental Science, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
⁷ Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305, USA; Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA; Veterans Affairs Palo Alto Health Care System, Palo Alto, CA 94304, USA. Electronic address: relman@stanford.edu.

PMID: 29153320
DOI: 10.1016/j.cub.2017.10.040

Abstract

The vast majority of bacterial diversity lies within phylum-level lineages called "candidate phyla," which lack isolated representatives and are poorly understood. These bacteria are surprisingly abundant in the oral cavity of marine mammals. We employed a genome-resolved metagenomic approach to recover and characterize genomes and functional potential from microbes in the oral gingival sulcus of two bottlenose dolphins (Tursiops truncatus). We detected organisms from 24 known bacterial phyla and one archaeal phylum. We also recovered genomes from two deep-branching, previously uncharacterized phylum-level lineages (here named "Candidatus Delphibacteria" and "Candidatus Fertabacteria"). The Delphibacteria lineage is found in both managed and wild dolphins; its metabolic profile suggests a capacity for denitrification and a possible role in dolphin health. We uncovered a rich diversity of predicted Cas9 proteins, including the two longest predicted Cas9 proteins to date. Notably, we identified the first type II CRISPR-Cas systems encoded by members of the Candidate Phyla Radiation. Using their spacer sequences, we subsequently identified and assembled a complete Saccharibacteria phage genome. These findings underscore the immense microbial diversity and functional potential that await discovery in previously unexplored environments.

Keywords: CRISPR; Cas9; Tursiops truncatus; bacteriophage; candidate phyla; dolphin; marine mammal; metagenomics; microbial ecology; oral microbiota.

Published by Elsevier Ltd.

MeSH terms

Animals
Archaea / classification*
Bacteria / classification*
Bottle-Nosed Dolphin / microbiology*
Female
Genome, Archaeal*
Genome, Bacterial*
Male
Metagenome*
Metagenomics
Microbiota*
Mouth / microbiology