Colony location and captivity influence the gut microbial community composition of the Australian sea lion (Neophoca cinerea)

Applied and Environmental Microbiology

Volumn 82, Issue 12, 2016, Pages 3440-3449

  Delport, Tiffany C ^a   Power, Michelle L ^a   Harcourt, Robert G ^a   Webster, Koa N ^a   Tetu, Sasha G ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; MARINE ENGINEERING; VETERINARY MEDICINE;

ANTHROPOGENIC DISTURBANCE; ANTHROPOGENIC IMPACTS; BACTERIAL COMMUNITY; BIOLOGICAL ENVIRONMENTS; MICROBIAL COMMUNITY COMPOSITION; OPERATIONAL TAXONOMIC UNITS; PRINCIPAL COORDINATE ANALYSIS; QUALITATIVE DIFFERENCES;

MAMMALS;

ANTHROPOGENIC EFFECT; BACTERIUM; CAPTIVITY; COMMUNITY COMPOSITION; ENDANGERED SPECIES; FECAL COLIFORM; FORAGING BEHAVIOR; IMMUNE SYSTEM; METABOLISM; MICROBIAL COMMUNITY; PINNIPED; SITE FIDELITY;

AUSTRALIA; WESTERN AUSTRALIA;

ACTINOBACTERIA; ANIMALIA; BACTERIA (MICROORGANISMS); BACTEROIDETES; CLOSTRIDIACEAE; FIRMICUTES; FUSOBACTERIA; MAMMALIA; NEOPHOCA CINEREA; PINNIPEDIA; PROTEOBACTERIA;

ANIMAL; AUSTRALIA; BACTERIUM; BIOTA; CLASSIFICATION; COMPARATIVE STUDY; FECES; GASTROINTESTINAL TRACT; GENETICS; GEOGRAPHY; MICROBIOLOGY; OTARIIDAE; WILD ANIMAL; ZOO ANIMAL;

ANIMALS; ANIMALS, WILD; ANIMALS, ZOO; AUSTRALIA; BACTERIA; BIOTA; FECES; GASTROINTESTINAL TRACT; GEOGRAPHY; SEA LIONS;

EID: 84971439959     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00192-16     Document Type: Article

References (55)

1. Bonde RK, Aguirre AA, Powell J. 2004. Manatees as sentinels of marine ecosystem health: are they the 2000-pound canaries? EcoHealth 1:255-262. http://dx.doi.org/10.1007/s10393-004-0095-5.
2. Cook PF, Reichmuth C, Rouse AA, Libby LA, Dennison SE, Carmichael OT, Kruse-Elliott KT, Bloom J, Singh B, Fravel VA, Barbosa L. 2015. Algal toxin impairs sea lion memory and hippocampal connectivity, with implications for strandings. Science 350:1545-1547. http://dx.doi.org/10.1126/science.aac5675.
3. Jessup D, Miller M, Ames J, Harris M, Kreuder C, Conrad PA, Mazet J. 2004. Southern sea otter as a sentinel of marine ecosystem health. Eco-Health 1:239-245. http://dx.doi.org/10.1007/s10393-004-0093-7.
4. Moore SE. 2008. Marine mammals as ecosystem sentinels. J Mammal 89:534-540. http://dx.doi.org/10.1644/07-MAMM-S-312R1.1.
5. Nelson TM, Rogers TL, Carlini AR, Brown MV. 2013. Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ Microbiol 15:1132-1145. http://dx.doi.org/10.1111/1462-2920.12022.
6. Wells RS, Rhinehart H, Hansen L, Sweeney J, Townsend F, Stone R, Casper DR, Scott M, Hohn A, Rowles T. 2004. Bottlenose dolphins as marine ecosystems sentinels: developing a health monitoring system. Eco-Health 1:246-254. http://dx.doi.org/10.1007/s10393-004-0094-6.
7. Apprill A, Robbins J, Eren AM, Pack AA, Reveillaud J, Matilla D, Moore M, Niemeyer M, Moore KTM, Mincer TJ. 2014. Humpback whale populations share a core skin bacterial community: towards a health index for marine mammals? PLoS One 9:e90785. http://dx.doi.org/10.1371/journal.pone.0090785.
8. Stappenbeck TS, Hooper LV, Gordon JI. 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad SciUSA99:15451-15455. http://dx.doi.org/10.1073/pnas.202604299.
9. Tremaroli V, Backhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249. http://dx.doi.org/10.1038/nature11552.
10. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G. 2009. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 106: 3698-3703. http://dx.doi.org/10.1073/pnas.0812874106.
11. Hooper LV, TM, Gordon JI. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283-307. http://dx.doi.org/10.1146/annurev.nutr.22.011602.092259.
12. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307:1915-1920. http://dx.doi.org/10.1126/science.1104816.
13. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI. 2008. Evolution of mammals and their gut microbes. Science 320:1647-1651. http://dx.doi.org/10.1126/science.1155725.
14. Yildirim S, Yeoman CJ, Sipos M, Torralba M, Wilson BA, Goldberg TL, Stumpf RM, Leigh SR, White BA, Nelson KE, Ii R, Martin R. 2010. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One 5:e13963. http://dx.doi.org/10.1371/journal.pone.0013963.
15. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI. 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970-974. http://dx.doi.org/10.1126/science.1198719.
16. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua K, Kachman SD, Moriyama EN, Walter J, Peterson DA, Pomp D. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad SciUSA107:18933-18938. http://dx.doi.org/10.1073/pnas.1007028107.
17. Nelson TM, Rogers TL, Brown MV. 2013. The gut bacterial community of mammals from marine and terrestrial habitats. PLoS One 8:e83655. http://dx.doi.org/10.1371/journal.pone.0083655.
18. Banks JC, Cary SC, Hogg ID. 2014. Isolated fecal bacterial communities found for Weddell seals, Leptonychotes weddellii, at White Island, Mc-Murdo Sound, Antarctica. Polar Biol 37:1857-1864. http://dx.doi.org/10.1007/s00300-014-1567-x.
19. Glad T, Kristiansen VF, Nielsen KM, Brusetti L, Wright AG, Sundset MA. 2010. Ecological characterization of the colonic microbiota in arctic and sub-arctic seals. Microb Ecol 60:323-330. http://dx.doi.org/10.1007/s00248-010-9690-x.
20. Lavery TJ, Roudnew B, Seymour J, Mitchell JG, Jeffries T. 2012. High nutrient transport and cycling potential revealed in the microbial metagenome of Australian sea lion (Neophoca cinerea) faeces. PLoS One 7:e36478. http://dx.doi.org/10.1371/journal.pone.0036478.
21. Smith SC, Chalker A, Dewar ML, Arnould JP. 2013. Age-related differences revealed in Australian fur seal Arctocephalus pusillus doriferus gut microbiota. FEMS Microbiol Ecol 86:246-255. http://dx.doi.org/10.1111/1574-6941.12157.
22. Shaughnessy PD, Goldsworthy SD, Hamer DJ, Page B, McIntosh RR. 2011. Australian sea lions Neophoca cinerea at colonies in South Australia: distribution and abundance, 2004 to 2008. Endang Species Res 13:87-98. http://dx.doi.org/10.3354/esr00317.
23. Ling JK. 2002. Impact of colonial sealing on seal stocks around Australia, New Zealand and subantarctic islands between 150 and 170 degrees east. Aust Mammal 24:117-126. http://dx.doi.org/10.1071/AM02117.
24. Shaughnessy PD, Dennis TE, Seager PG. 2005. Status of Australian sea lions, Neophoca cinerea, and New Zealand fur seals, Arctocephalus forsteri, on Eyre Peninsula and the far west coast of South Australia. Wildl Res 32:85-101. http://dx.doi.org/10.1071/WR03068.
25. Lowther AD, Harcourt RG, Goldsworthy SD. 2013. Regional variation in trophic ecology of adult female Australian sea lions inferred from stable isotopes in whiskers. Wildl Res 40:303-311. http://dx.doi.org/10.1071/WR12181.
26. Lowther AD, Harcourt RG, Goldsworthy SD, Stow AJ. 2012. Population structure of adult female Australian sea lions is driven by fine-scale foraging site fidelity. Anim Behav 83:691-701. http://dx.doi.org/10.1016/j.anbehav.2011.12.015.
27. Gales NJ, Cheal AJ. 1992. Estimating diet composition of the Australian sea-lion (Neophoca cinerea) from scat analysis: an unreliable technique. Wildl Res 19:447-456. http://dx.doi.org/10.1071/WR9920447.
28. McIntosh RR, Page B, Goldsworthy SD. 2007. Dietary analysis of regurgitates and stomach samples from free-living Australian sea lions. Wildl Res 33:661-669. http://dx.doi.org/10.1071/wr06025.
29. Goldsworthy SD, Shaughnessy PD, Page B, McIntosh RR, Hamer DJ, Peters KJ, Baylis AM, Lowther AD, Bradshaw CJ. 2007. Developing population monitoring protocols of Australia sea-lions. SARDI Res Rep Ser no. 219. SARDI Aquatic Sciences, Adelaide, SA, Australia.
30. Delport TC, Harcourt RG, Beaumont LJ, Webster KN, Power ML. 2015. Molecular detection of antibiotic-resistance determinants in Escherichia coli isolated from the endangered Australian sea lion (Neophoca cinerea). J Wildl Dis 51:555-563. http://dx.doi.org/10.7589/2014-08-200.
31. Bossart GD. 2006. Marine mammals as sentinel species for oceans and human health. Oceanography 19:44-47. http://dx.doi.org/10.5670/oceanog.2006.77.
32. Walker GE, Ling JK. 1981. New Zealand sea lion Phocarctos hookeri (Gray, 1844), p 25-38. In Ridgway SH, Harrison RJ (ed), Handbook of marine mammals, vol 1. The walrus, sea lions, fur seals and sea otter. Academic Press, London, United Kingdom.
33. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621-1624. http://dx.doi.org/10.1038/ismej.2012.8.
34. Lane DJ. 1991. Nucleic acid techniques in bacterial systematics. John Wiley & Sons, New York, NY.
35. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
36. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
37. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069-5072. http://dx.doi.org/10.1128/AEM.03006-05.
38. Environmental Systems Resource Institute. 2010. ArcGIS, version 10.0. Environmental Systems Resource Institute, Redlands, CA.
39. Hammer Ø, Harper DAT, Ryan PD. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9.
40. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101:15718-15723. http://dx.doi.org/10.1073/pnas.0407076101.
41. Pabst DA, Rommel SA, McLellan WA. 1999. The functional morphology of marine mammals. In Biology of marine mammals. Melbourne University Press, Melbourne, Australia.
42. Lombardo MP. 2008. Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living. Behav Ecol Sociobiol 62:479-497. http://dx.doi.org/10.1007/s00265-007-0428-9.
43. Shaughnessy P. 2007. Lilliput Island (small North-east Franklin Islet), Eyre Peninsula, South Australia. Corella 31:83-84.
44. Shaughnessy P, Dennis T, Armstrong D, Berris S. 2008. Landbirds of three islands off the west coast of Eyre Peninsula, South Australia: Lilliput, Nicolas Baudin and West Waldegrave. Corella 32:17-19.
45. Nelson M, Jones SH, Edwards C, Ellis JC. 2008. Characterization of Escherichia coli populations from gulls, landfill trash, and wastewater using ribotyping. Dis Aquat Organ 81:53-63. http://dx.doi.org/10.3354/dao01937.
46. Campbell RA, Gales NJ, Lento GM, Baker CS. 2008. Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea. Biol Lett 4:139-142. http://dx.doi.org/10.1098/rsbl.2007.0487.
47. Dhanasiri AK, Brunvold L, Brinchmann MF, Korsnes K, Bergh O, Kiron V. 2011. Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing. Microb Ecol 61:20-30. http://dx.doi.org/10.1007/s00248-010-9673-y.
48. Ellison MJ, Conant GC, Cockrum RR, Austin KJ, Truong H, Becchi M, Lamberson WR, Cammack KM. 2014. Diet alters both the structure and taxonomy of the ovine gut microbial ecosystem. DNA Res 21:115-125. http://dx.doi.org/10.1093/dnares/dst044.
49. Kohl KD, Dearing MD. 2014. Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity. Environ Microbiol Rep 6:191-195. http://dx.doi.org/10.1111/1758-2229.12118.
50. Kopecnỳ J, Hodrová B, Stewart CS. 1996. The isolation and characterization of a rumen chitinolytic bacterium. Lett Appl Microbiol 23: 195-198.
51. Kopecnỳ J, Hodrová B. 2000. Chitinolytic enzymes produced by ovine rumen bacteria. Folia Microbiol (Praha) 45:465-468. http://dx.doi.org/10.1007/BF02817622.
52. Simůnek J, Kopecnỳ J, Hodrová B, Bartonová H. 2002. Identification and characterization of Clostridium paraputrificum, a chitinolytic bacterium of human digestive tract. Folia Microbiol (Praha) 47:559-564. http://dx.doi.org/10.1007/BF02818798.
53. Stoddard RA, Atwill ER, Conrad PA, Byrne BA, Jang S, Lawrence J, McCowan B, Gulland FM. 2009. The effect of rehabilitation of northern elephant seals (Mirounga angustirostris) on antimicrobial resistance of commensal Escherichia coli. Vet Microbiol 133:264-271. http://dx.doi.org/10.1016/j.vetmic.2008.07.022.
54. Castinel A, Kittelberger R, Pomroy WE, Duignan PJ, Chilvers BL, Wilkinson IS. 2008. Humoral immune response to Klebsiella spp. in New Zealand sea lions (Phocarctos hookeri) and the passive transfer of immunity to pups. J Wildl Dis 44:8-15. http://dx.doi.org/10.7589/0090-3558-44.1.8.
55. Delport TC, Asher AJ, Beaumont LJ, Webster KN, Harcourt RG, Power ML. 2014. Giardia duodenalis and Cryptosporidium occurrence in Australian sea lions (Neophoca cinerea) exposed to varied levels of human interaction. Int J Parasitol Parasites Wildl 3:269-275. http://dx.doi.org/10.1016/j.ijppaw.2014.09.001.