DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

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. Here 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. Finally, these findings underscore the immense microbial diversity and functional potential that await discovery in previously unexplored environments.

Authors:
 [1];  [2];  [3];  [3];  [2];  [2];  [3];  [4];  [5]
  1. University of California, Santa Cruz, CA (United States)
  2. Stanford University, CA (United States)
  3. University of California, Berkeley, CA (United States)
  4. University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  5. Stanford University, CA (United States); Veterans Affairs Palo Alto Health Care System, Palo Alto, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE; US Department of the Navy, Office of Naval Research (ONR); Allen Institute; Fonds de recherche du Québec – Nature et technologies (FRQNT); Thomas C. and Joan M. Merigan Endowment at Stanford University
OSTI Identifier:
1487293
Alternate Identifier(s):
OSTI ID: 1479361
Grant/Contract Number:  
AC02-05CH11231; 00014-07-1-0287
Resource Type:
Published Article
Journal Name:
Current Biology
Additional Journal Information:
Journal Volume: 27; Journal Issue: 24; Journal ID: ISSN 0960-9822
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; oral microbiota; microbial ecology; candidate phyla; metagenomics; Tursiops truncatus; dolphin; marine mammal; CRISPR; Cas9; bacteriophage

Citation Formats

Dudek, Natasha K., Sun, Christine L., Burstein, David, Kantor, Rose S., Aliaga Goltsman, Daniela S., Bik, Elisabeth M., Thomas, Brian C., Banfield, Jillian F., and Relman, David A. Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome. United States: N. p., 2017. Web. doi:10.1016/j.cub.2017.10.040.
Dudek, Natasha K., Sun, Christine L., Burstein, David, Kantor, Rose S., Aliaga Goltsman, Daniela S., Bik, Elisabeth M., Thomas, Brian C., Banfield, Jillian F., & Relman, David A. Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome. United States. https://doi.org/10.1016/j.cub.2017.10.040
Dudek, Natasha K., Sun, Christine L., Burstein, David, Kantor, Rose S., Aliaga Goltsman, Daniela S., Bik, Elisabeth M., Thomas, Brian C., Banfield, Jillian F., and Relman, David A. Thu . "Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome". United States. https://doi.org/10.1016/j.cub.2017.10.040.
@article{osti_1487293,
title = {Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome},
author = {Dudek, Natasha K. and Sun, Christine L. and Burstein, David and Kantor, Rose S. and Aliaga Goltsman, Daniela S. and Bik, Elisabeth M. and Thomas, Brian C. and Banfield, Jillian F. and Relman, David A.},
abstractNote = {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. Here 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. Finally, these findings underscore the immense microbial diversity and functional potential that await discovery in previously unexplored environments.},
doi = {10.1016/j.cub.2017.10.040},
journal = {Current Biology},
number = 24,
volume = 27,
place = {United States},
year = {2017},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.cub.2017.10.040

Citation Metrics:
Cited by: 46 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A new view of the tree of life
journal, April 2016


Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs
journal, January 2016

  • Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10476

Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015

  • Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C.
  • Nature, Vol. 523, Issue 7559
  • DOI: 10.1038/nature14486

Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla
journal, October 2013


First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking
journal, January 2015

  • Sekiguchi, Yuji; Ohashi, Akiko; Parks, Donovan H.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.740

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle
journal, December 2014

  • He, Xuesong; McLean, Jeffrey S.; Edlund, Anna
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
  • DOI: 10.1073/pnas.1419038112

New CRISPR–Cas systems from uncultivated microbes
journal, December 2016

  • Burstein, David; Harrington, Lucas B.; Strutt, Steven C.
  • Nature, Vol. 542, Issue 7640
  • DOI: 10.1038/nature21059

A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea
journal, December 2009

  • Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos
  • Nature, Vol. 462, Issue 7276
  • DOI: 10.1038/nature08656

Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea
journal, February 2016

  • Bik, Elisabeth M.; Costello, Elizabeth K.; Switzer, Alexandra D.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10516

SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
journal, November 2007

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks
journal, November 2013

  • Yilmaz, Pelin; Parfrey, Laura Wegener; Yarza, Pablo
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1209

Archaea on Human Skin
journal, June 2013


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
journal, August 2014

  • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
  • Nature Reviews Microbiology, Vol. 12, Issue 9
  • DOI: 10.1038/nrmicro3330

A Systematic Analysis of Biosynthetic Gene Clusters in the Human Microbiome Reveals a Common Family of Antibiotics
journal, September 2014


The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease
journal, April 2008

  • Kadioglu, Aras; Weiser, Jeffrey N.; Paton, James C.
  • Nature Reviews Microbiology, Vol. 6, Issue 4
  • DOI: 10.1038/nrmicro1871

antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences
journal, June 2011

  • Medema, Marnix H.; Blin, Kai; Cimermancic, Peter
  • Nucleic Acids Research, Vol. 39, Issue suppl_2
  • DOI: 10.1093/nar/gkr466

antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers
journal, May 2013

  • Blin, Kai; Medema, Marnix H.; Kazempour, Daniyal
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt449

antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters
journal, May 2015

  • Weber, Tilmann; Blin, Kai; Duddela, Srikanth
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv437

Minimum Information about a Biosynthetic Gene cluster
journal, August 2015

  • Medema, Marnix H.; Kottmann, Renzo; Yilmaz, Pelin
  • Nature Chemical Biology, Vol. 11, Issue 9
  • DOI: 10.1038/nchembio.1890

Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation
journal, November 2015

  • O'Leary, Nuala A.; Wright, Mathew W.; Brister, J. Rodney
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1189

The HHpred interactive server for protein homology detection and structure prediction
journal, July 2005

  • Soding, J.; Biegert, A.; Lupas, A. N.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki408

The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015

  • Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
  • Nature Protocols, Vol. 10, Issue 6
  • DOI: 10.1038/nprot.2015.053

Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems
journal, February 2016

  • Burstein, David; Sun, Christine L.; Brown, Christopher T.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10613

Accurate, multi-kb reads resolve complex populations and detect rare microorganisms
journal, February 2015

  • Sharon, Itai; Kertesz, Michael; Hug, Laura A.
  • Genome Research, Vol. 25, Issue 4
  • DOI: 10.1101/gr.183012.114

Uncovering Earth’s virome
journal, August 2016

  • Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
  • Nature, Vol. 536, Issue 7617
  • DOI: 10.1038/nature19094

CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007

  • Grissa, I.; Vergnaud, G.; Pourcel, C.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm360

Crass: identification and reconstruction of CRISPR from unassembled metagenomic data
journal, March 2013

  • Skennerton, Connor T.; Imelfort, Michael; Tyson, Gene W.
  • Nucleic Acids Research, Vol. 41, Issue 10
  • DOI: 10.1093/nar/gkt183

The nitrate–nitrite–nitric oxide pathway in physiology and therapeutics
journal, February 2008

  • Lundberg, Jon O.; Weitzberg, Eddie; Gladwin, Mark T.
  • Nature Reviews Drug Discovery, Vol. 7, Issue 2
  • DOI: 10.1038/nrd2466

Denitrification in human dental plaque
journal, March 2010


Prevalence of Bacteria of Division TM7 in Human Subgingival Plaque and Their Association with Disease
journal, March 2003


A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity
journal, June 2012


ABCdb: an online resource for ABC transporter repertories from sequenced archaeal and bacterial genomes: ABCdb: transporter repertoires
journal, March 2006


A high-resolution map of human evolutionary constraint using 29 mammals
journal, October 2011

  • Lindblad-Toh, Kerstin; Garber, Manuel; Zuk, Or
  • Nature, Vol. 478, Issue 7370
  • DOI: 10.1038/nature10530

KEGG as a reference resource for gene and protein annotation
journal, October 2015

  • Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1070

KEGG: new perspectives on genomes, pathways, diseases and drugs
journal, November 2016

  • Kanehisa, Minoru; Furumichi, Miho; Tanabe, Mao
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1092

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

NCBI Viral Genomes Resource
journal, November 2014

  • Brister, J. Rodney; Ako-adjei, Danso; Bao, Yiming
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1207

PATRIC, the bacterial bioinformatics database and analysis resource
journal, November 2013

  • Wattam, Alice R.; Abraham, David; Dalay, Oral
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1099

UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches
journal, November 2014


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Circos: An information aesthetic for comparative genomics
journal, June 2009


HMMER web server: 2015 update
journal, May 2015

  • Finn, Robert D.; Clements, Jody; Arndt, William
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv397

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


InterProScan 5: genome-scale protein function classification
journal, January 2014


Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011

  • Letunic, I.; Bork, P.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr201

KAAS: an automatic genome annotation and pathway reconstruction server
journal, May 2007

  • Moriya, Y.; Itoh, M.; Okuda, S.
  • Nucleic Acids Research, Vol. 35, Issue S2, p. W182-W185
  • DOI: 10.1093/nar/gkm321

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

PRICE: Software for the Targeted Assembly of Components of (Meta) Genomic Sequence Data
journal, March 2013

  • Ruby, J. Graham; Bellare, Priya; DeRisi, Joseph L.
  • G3: Genes|Genomes|Genetics, Vol. 3, Issue 5
  • DOI: 10.1534/g3.113.005967

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


ProtTest 3: fast selection of best-fit models of protein evolution
journal, February 2011


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
journal, May 2012


tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Community-wide analysis of microbial genome sequence signatures
journal, January 2009

  • Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J.
  • Genome Biology, Vol. 10, Issue 8
  • DOI: 10.1186/gb-2009-10-8-r85

A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood
journal, October 2003


The Pfam protein families database: towards a more sustainable future
journal, December 2015

  • Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1344

Accelerated Profile HMM Searches
journal, October 2011


An updated evolutionary classification of CRISPR–Cas systems
journal, September 2015

  • Makarova, Kira S.; Wolf, Yuri I.; Alkhnbashi, Omer S.
  • Nature Reviews Microbiology, Vol. 13, Issue 11, p. 722-736
  • DOI: 10.1038/nrmicro3569

CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


Discovery and Functional Characterization of Diverse Class 2 CRISPR-Cas Systems
journal, November 2015


Works referencing / citing this record:

The distinction of CPR bacteria from other bacteria based on protein family content
journal, September 2019


Microbiota fingerprints within the oral cavity of cetaceans as indicators for population biomonitoring
journal, September 2019

  • Soares-Castro, Pedro; Araújo-Rodrigues, Helena; Godoy-Vitorino, Filipa
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-019-50139-7

Candidate Phyla Radiation Roizmanbacteria From Hot Springs Have Novel and Unexpectedly Abundant CRISPR-Cas Systems
journal, May 2019