Marine Mammals Harbor Unique Microbiotas Shaped by and Yet Distinct from the Sea

Overview

Journal Nat Commun

Specialty Biology

Date 2016 Feb 4

PMID 26839246

Citations 95

Authors

Elisabeth M Bik

Elizabeth K Costello

Alexandra D Switzer

Benjamin J Callahan

Susan P Holmes

Randall S Wells

Kevin P Carlin

Eric D Jensen

Stephanie Venn-Watson

David A Relman

Affiliations

Soon will be listed here.

Abstract

Marine mammals play crucial ecological roles in the oceans, but little is known about their microbiotas. Here we study the bacterial communities in 337 samples from 5 body sites in 48 healthy dolphins and 18 healthy sea lions, as well as those of adjacent seawater and other hosts. The bacterial taxonomic compositions are distinct from those of other mammals, dietary fish and seawater, are highly diverse and vary according to body site and host species. Dolphins harbour 30 bacterial phyla, with 25 of them in the mouth, several abundant but poorly characterized Tenericutes species in gastric fluid and a surprisingly paucity of Bacteroidetes in distal gut. About 70% of near-full length bacterial 16S ribosomal RNA sequences from dolphins are unique. Host habitat, diet and phylogeny all contribute to variation in marine mammal distal gut microbiota composition. Our findings help elucidate the factors structuring marine mammal microbiotas and may enhance monitoring of marine mammal health.

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References

Smith S, Chalker A, Dewar M, Arnould J . Age-related differences revealed in Australian fur seal Arctocephalus pusillus doriferus gut microbiota. FEMS Microbiol Ecol. 2013; 86(2):246-55. DOI: 10.1111/1574-6941.12157. View

Suchodolski J, Camacho J, Steiner J . Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microbiol Ecol. 2008; 66(3):567-78. DOI: 10.1111/j.1574-6941.2008.00521.x. View

Russell V, Hold G, Pryde S, Rehbein H, Quinteiro J, Rey-Mendez M . Use of restriction fragment length polymorphism to distinguish between salmon species. J Agric Food Chem. 2000; 48(6):2184-8. DOI: 10.1021/jf991213e. View

Johnson W, Torralba M, Fair P, Bossart G, Nelson K, Morris P . Novel diversity of bacterial communities associated with bottlenose dolphin upper respiratory tracts. Environ Microbiol Rep. 2013; 1(6):555-62. DOI: 10.1111/j.1758-2229.2009.00080.x. View

DeSantis T, Hugenholtz P, Larsen N, Rojas M, Brodie E, Keller K . Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72(7):5069-72. PMC: 1489311. DOI: 10.1128/AEM.03006-05. View

Dewhirst F, Klein E, Thompson E, Blanton J, Chen T, Milella L . The canine oral microbiome. PLoS One. 2012; 7(4):e36067. PMC: 3338629. DOI: 10.1371/journal.pone.0036067. View

Foote A, Liu Y, Thomas G, Vinar T, Alfoldi J, Deng J . Convergent evolution of the genomes of marine mammals. Nat Genet. 2015; 47(3):272-5. PMC: 4644735. DOI: 10.1038/ng.3198. View

Palmer C, Bik E, DiGiulio D, Relman D, Brown P . Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5(7):e177. PMC: 1896187. DOI: 10.1371/journal.pbio.0050177. View

Meredith R, Janecka J, Gatesy J, Ryder O, Fisher C, Teeling E . Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science. 2011; 334(6055):521-4. DOI: 10.1126/science.1211028. View

10.

Turnbaugh P, Backhed F, Fulton L, Gordon J . Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008; 3(4):213-23. PMC: 3687783. DOI: 10.1016/j.chom.2008.02.015. View

11.

DeSantis Jr T, Hugenholtz P, Keller K, Brodie E, Larsen N, Piceno Y . NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 2006; 34(Web Server issue):W394-9. PMC: 1538769. DOI: 10.1093/nar/gkl244. View

12.

Costello E, Lauber C, Hamady M, Fierer N, Gordon J, Knight R . Bacterial community variation in human body habitats across space and time. Science. 2009; 326(5960):1694-7. PMC: 3602444. DOI: 10.1126/science.1177486. View

13.

Zhang H, Chen L . Phylogenetic analysis of 16S rRNA gene sequences reveals distal gut bacterial diversity in wild wolves (Canis lupus). Mol Biol Rep. 2010; 37(8):4013-22. DOI: 10.1007/s11033-010-0060-z. View

14.

Morris P, Johnson W, Pisani J, Bossart G, Adams J, Reif J . Isolation of culturable microorganisms from free-ranging bottlenose dolphins (Tursiops truncatus) from the southeastern United States. Vet Microbiol. 2010; 148(2-4):440-7. DOI: 10.1016/j.vetmic.2010.08.025. View

15.

Thakuria D, Schmidt O, Finan D, Egan D, Doohan F . Gut wall bacteria of earthworms: a natural selection process. ISME J. 2009; 4(3):357-66. DOI: 10.1038/ismej.2009.124. View

16.

Harper C, Feng Y, Xu S, Taylor N, Kinsel M, Dewhirst F . Helicobacter cetorum sp. nov., a urease-positive Helicobacter species isolated from dolphins and whales. J Clin Microbiol. 2002; 40(12):4536-43. PMC: 154630. DOI: 10.1128/JCM.40.12.4536-4543.2002. View

17.

Glad T, Kristiansen V, Nielsen K, Brusetti L, Wright A, Sundset M . Ecological characterisation of the colonic microbiota in arctic and sub-arctic seals. Microb Ecol. 2010; 60(2):320-30. DOI: 10.1007/s00248-010-9690-x. View

18.

Glad T, Bernhardsen P, Nielsen K, Brusetti L, Andersen M, Aars J . Bacterial diversity in faeces from polar bear (Ursus maritimus) in Arctic Svalbard. BMC Microbiol. 2010; 10:10. PMC: 2822771. DOI: 10.1186/1471-2180-10-10. View

19.

Nelson T, Rogers T, Brown M . The gut bacterial community of mammals from marine and terrestrial habitats. PLoS One. 2014; 8(12):e83655. PMC: 3875473. DOI: 10.1371/journal.pone.0083655. View

20.

Brown C, Hug L, Thomas B, Sharon I, Castelle C, Singh A . Unusual biology across a group comprising more than 15% of domain Bacteria. Nature. 2015; 523(7559):208-11. DOI: 10.1038/nature14486. View