Humpback whale populations share a core skin bacterial community: Towards a health index for marine mammals?

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Apprill, Amy ^a   Robbins, Jooke ^b   Eren, A Murat ^c   Pack, Adam A ^d,e   Reveillaud, Julie ^c   Mattila, David ^f   Moore, Michael ^a   Niemeyer, Misty ^g   Moore, Kathleen M T ^g   Mincer, Tracy J ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b CENTER FOR COASTAL STUDIES   (United States)

^c MARINE BIOLOGICAL LABORATORY   (United States)

^d UNIVERSITY OF HAWAII AT HILO   (United States)

^e Dolphin Institute   (United States)

^f Hawaiian Islands Humpback Whale National Marine Sanctuary   (United States)

^g INTERNATIONAL FUND FOR ANIMAL WELFARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ALPHAPROTEOBACTERIA; ANATOMICAL CONCEPTS; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL METABOLISM; FIRMICUTES; GAMMAPROTEOBACTERIA; HUMPBACK WHALE; MEGAPTERA NOVAEANGLIAE; MICROBIAL COMMUNITY; MICROBIAL IDENTIFICATION; MICROBIAL VIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION ABUNDANCE; SKIN FLORA; SPECIES RICHNESS; TENACIBACULUM; ANALYSIS OF VARIANCE; ANIMAL; AQUATIC SPECIES; BACTERIUM; BIODIVERSITY; CLASSIFICATION; FEMALE; GENETICS; GEOGRAPHY; HEALTH; MALE; MICROBIOLOGY; MICROFLORA; SKIN; ULTRASTRUCTURE;

RIBOSOME RNA;

ANALYSIS OF VARIANCE; ANIMALS; AQUATIC ORGANISMS; BACTERIA; BASE SEQUENCE; BIODIVERSITY; FEMALE; GEOGRAPHY; HEALTH; HUMPBACK WHALE; MALE; MICROBIOTA; PHYLOGENY; RNA, RIBOSOMAL; SKIN;

EID: 84899981109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090785     Document Type: Article

References (67)

1. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, et al. (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139: 1844-1854.e1841.
2. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, et al. (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences of the United States of America 10: 3698-3703.
3. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, et al. (2008) Evolution of mammals and their gut microbes. Science 320: 1647-1651. (Pubitemid 351931256)
4. Bowers RM, McCubbin IB, Hallar AG, Fierer N (2012) Seasonal variability in airborne bacterial communities at a high-elevation site. Atmospheric Environment 50: 41-49.
5. DeLong EF, Taylor LT, Marsh T, Preston CM (1999) Visualization and enumeration of marine planktonic Archaea and Bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl Environ Microb 65: 5554-5563. (Pubitemid 129520650)
6. Bernhardt AE, Colbert D, McManus J, Field KG (2005) Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries. FEMS Microbiology Ecology 51: 115-128. (Pubitemid 40261304)
7. Yeo SK, Huggett MJ, Eiler A, Rappé MS (2013) Coastal bacterioplankton community dynamics in response to a natural disturbance. PLoS ONE 8: e56207.
8. Apprill A, Mooney TA, Lyman E, Stimpert AK, Rappé MS (2011) Humpback whales harbour a combination of specific and variable skin bacteria. Environmental Microbiology Reports 3: 223-232.
9. Douglas AE (1998) Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera. Annual Review of Entomology 43: 17-37.
10. Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137: 506-523.
11. Fleming A, Jackson J (2011) Global review of humpback whales (Megaptera novaeangliae). In: U.S. Department of Commerce NOAA, National Marine Fisheries Service, Southwest Fisheries Science Center, editor. NOAA Technical Memorandum NMFS.
12. Clapham PJ (2000) The humpback whale: seasonal feeding and breeding in a baleen whale. In: Mann J, Connor RC, Tyack PL, Whitehead H, editors. Cetacean socities: field studies of dolphins and whales. Chicago: University of Chicago Press. pp. 173-196.
13. Baker CS, Herman LM, Perry A, Lawton WS, Straley JM, et al. (1986) Migratory movement and population structure of humpback whales (Megaptera novaeangliae) in the Central and Eastern North Pacific. Marine Ecology Progress Series 31: 105-119.
14. Chittleborough RG (1965) Dynamics of two populations of the humpback whale Megaptera novaeangliae (Borowski). Australian Journal of Marine and Freshwater Research 16: 33-128.
15. Craig AS, Herman LM, Gabriele CM, Pack AA (2003) Migratory timing of humpback whales (Megaptera novaeangliae) in the central North Pacific varies with age, sex and reproductive status. Behaviour 140: 981-1001. (Pubitemid 38038799)
16. Dawbin WH (1966) The seasonal migratory cycle of humpback whales. In: Norris KS, editor. Whales, dolphins and porpoises. Berkeley: University of California Press. pp. 145-170.
17. Katona S, Beard JA (1990) Population size, migrations, and feeding aggregations of the humpback whale (Megaptera novaeangliae) in the western Atlantic. Report of the International Whaling Committee Special Issue 12: 295-305.
18. Robbins J, Dalla Rosa L, Allen JM, Mattila DK, Secchi ER, et al. (2011) Return movement of a humpback whale between the Antarctic Peninsula and American Samoa: a seasonal migration record. Endangered Species Research 13: 117-121.
19. Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, et al. (2012) Environmental biodiversity, human microbiota, and allergy are interrelated. Proceedings of the National Academy of Sciences.
20. Scharschmidt TC, Fischbach MA (2013) What lives on our skin: ecology, genomics and therapeutic opportunities of the skin microbiome. Drug Discovery Today: Disease Mechanisms 10: e83-e89.
21. Harrison RJ, Thurley KW (1974) Structure of the epidermis in Tursiops, Delphinus and Phocoena. In: Harrison RJ, editor. Functional anatomy of marine mammals. London and New York: Academic Press. pp. 45-71.
22. Geraci JR, St. Aubin DJ, Hicks BD (1986) The epidermis of odontocetes: a vew from within. In: Bryden MM, Harrison R, editors. Research on Dolphins. Oxford: Clarendon Press. pp. 3-21.
23. Mouton M, Botha A (2012) Cutaneous Lesions in Cetaceans: An Indicator of Ecosystem Status?
24. Palsbøll P, Larsen F, Hansen E (1991) Sampling of skin biopsies from free-ranging large cetaceans in West Greenland: Development of new biopsy tips and bolt designs. Report of the International Whaling Committee Special Issue 13: 71-79.
25. Clapham PJ, Palsbøll PJ, Mattila DK (1993) High energy behaviors in humpback whales as a source of sloughed skin for molecular analysis. Marine Mammal Science 9: 214-220.
26. Bérubé M, Palsbøll PJ (1996) Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers: erratum. Molecular Ecology 5: 602.
27. Glockner DA, Venus S. Determining the sex of humpback whales (Megaptera novaeangliae) in their natural environment; 1983. pp. 447-464.
28. Apprill A, Hughen K, Mincer TJ (2013) Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environmental Microbiology 15: 2063-2072.
29. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
30. Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
31. Schloss PD (2010) The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6: e1000844.
32. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37: D141-D145.
33. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371. (Pubitemid 38854737)
34. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
35. Johnson WR, Torralba M, Fair PA, Bossart GD, Nelson KE, et al. (2009) Novel diversity of bacterial communities associated with bottlenose dolphin upper respiratory tracts. Environmental Microbiology Reports 1: 555-562.
36. Eren AM, Maignien L, Sul WJ, Murphy LG, Grim SL, et al. (2013) Oligotyping: Differentiating between closely related microbial taxa using 16S rRNA gene data. Methods in Ecology and Evolution 4: 1111-1119.
37. Eren AM, Zozaya M, Taylor CM, Dowd SE, Martin DH, et al. (2011) Exploring the Diversity of Gardnerella vaginalis in the Genitourinary Tract Microbiota of Monogamous Couples Through Subtle Nucleotide Variation. PLoS ONE 6: e26732.
38. McLellan SL, Newton RJ, Vandewalle JL, Shanks OC, Huse SM, et al. (2013) Sewage reflects the distribution of human faecal Lachnospiraceae. Environmental Microbiology 15: 2213-2227.
39. Clarke KR, Warwick RM (2001) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth: PRIMER-E.
40. McCune B, Grace J (2002) Analysis of ecological communities. Gleneden Beach, Oregon MJM Software Design. 304 p.
41. Frette L, Jorgensen NOG, Irming H, Kroer N (2004) Tenacibaculum skagerrakense sp. nov., a marine bacterium isolated from the pelagic zone in Skagerrak, Denmark. International Journal of Systematic and Evolutionary Microbiology 54: 519-524. (Pubitemid 38443751)
42. Yoon J-H, Kang S-J, Oh T-K (2005) Tenacibaculum lutimaris sp., nov., isolated from a tidal flat in the Yellow Sea, Korea. Int J Syst Evol Microbiol 55: 793-798. (Pubitemid 40485072)
43. Choi DH, Kim Y-G, Hwang CY, Yi H, Chun J, et al. (2006) Tenacibaculum litoreum sp. nov., isolated from tidal flat sediment. International Journal of Systematic and Evolultionary Microbiology 56: 635-640.
44. Jung S-Y, Oh T-K, Yoon J-H (2006) Tenacibaculum aestuarii sp. nov., isolated from a tidal flat sediment in Korea. International Journal of Systematic and Evolutionary Microbiology 56: 1577-1581. (Pubitemid 44097168)
45. Heindl H, Wiese J, Imhoff JF (2008) Tenacibaculum adriaticum sp. nov., from a bryozoan in the Adriatic Sea. International Journal of Systematic and Evolutionary Microbiology 58: 542-547.
46. Wang J-T, Chou Y-J, Chou J-H, Chen CA, Chen W-M (2008) Tenacibaculum aiptasiae sp. nov., isolated from a sea anemone Aiptasia pulchella. International Journal of Systematic and Evolutionary Microbiology 58: 761-766.
47. Piñeiro-Vidal M, Carballas CG, Gomez-Barreiro O, Riaza A, Santos Y (2008) Tenacibaculum soleae sp. nov., isolated from diseased sole (Solea senegalensis Kaup). International Journal of Systematic and Evolutionary Microbiology 58: 881- 885.
48. Piñeiro-Vidal M, Gijón D, Zarza C, Santos Y (2012) Tenacibaculum dicentrarchi sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from European sea bass. International Journal of Systematic and Evolutionary Microbiology 62: 425-429.
49. Piñeiro-Vidal M, Riaza A, Santos Y (2008) Tenacibaculum discolor sp. nov. and Tenacibaculum gallaicum sp. nov., isolated from sole (Solea senegalensis) and turbot (Psetta maxima) culture systems. International Journal of Systematic and Evolutionary Microbiology 58: 21-25. (Pubitemid 351843532)
50. Banning E, Casciotti K, Kujawinski E (2010) Novel strains isolated from a coastal aquifer suggest a predatory role for Flavobacteria. FEMS Microbiology Ecology 73: 254-270.
51. Bowman JP, Cavanagh J, Austin JJ, Sanderson K (1996) Novel Psychrobacter Species from Antarctic Ornithogenic Soils. International Journal of Systematic Bacteriology 46: 841-848. (Pubitemid 26339201)
52. Bowman JP, Nichols DS, McMeekin TA (1997) Psychrobacter glacincola sp. nov., a Halotolerant, Psychrophilic Bacterium Isolated from Antarctic Sea Ice. Systematic and Applied Microbiology 20: 209-215. (Pubitemid 27352907)
53. Denner EBM, Mark B, Mark B, Busse H-J, Busse H-J, et al. (2001) Psychrobacter proteolyticus sp. nov., a Psychrotrophic, Halotolerant Bacterium Isolated from the Antarctic Krill Euphausia superba Dana, Excreting a Cold-Adapted Metalloprotease. Systematic and Applied Microbiology 24: 44-53. (Pubitemid 32433692)
54. Romanenko LA, Schumann P, Rohde M, Lysenko AM, Mikhailov VV, et al. (2002) Psychrobacter submarinus sp. nov. and Psychrobacter marincola sp. nov., psychrophilic halophiles from marine environments. International Journal of Systematic and Evolutionary Microbiology 52: 1291-1297. (Pubitemid 34846429)
55. Ayala-del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N, et al. (2010) The Genome Sequence of Psychrobacter arcticus 273-4, a Psychroactive Siberian Permafrost Bacterium, Reveals Mechanisms for Adaptation to Low-Temperature Growth. Applied and Environmental Microbiology 76: 2304-2312.
56. Mathieu A, Delmont TO, Vogel TM, Robe P, Nalin R, et al. (2013) Life on Human Surfaces: Skin Metagenomics. PLoS ONE 8: e65288.
57. Costello EK, Gordon JI, Secor SM, Knight R (2010) Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J 4: 1375-1385.
58. Nixon PGF (1989) Human functions and the Heart. In: Seedhouse D, Cribb A, editors. Changing Ideas in Health Care. New York: John Wiley and Sons.
59. Demling RH (2009) Nutrition, Anabolism, and the Wound Healing Process: An Overview. Eplasty 9: e9.
60. Grice EA, Segre JA (2011) The skin microbiome. Nature Reviews Microbiology 9: 244-253.
61. Brown WR, Geraci JR, Hicks BD, St.-Aubin DJ, Schroeder JP (1983) Epidermal cell proliferation in the bottlenose dolphin (Tursiops truncatus). Canadian Journal of Zoology 61: 1587-1590.
62. Hicks BD, St. Aubin DJ, Geraci JR, Brown WR (1985) Epidermal growth in the bottlenose dolphin, Tursiops truncatus. Journal of Investigative Dermatology 85: 60-65.
63. Zabka TS, Romano TA (2003) Distribution of MHC II (+) cells in skin of the Atlantic bottlenose dolphin (Tursiops truncatus): An initial investigation of dolphin dendritic cells. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology 273A: 636-647. (Pubitemid 37408356)
64. Cassoff RM, Moore KM, McLellan WA, Barco SG, Rotstein DS, et al. (2011) Lethal entanglement in baleen whales. Diseases of Aquatic Organisms 96: 175-185.
65. Gulland FMD, Nutter FB, Dixon K, Calambokidis J, Schorr G, et al. (2008) Health Assessment, Antibiotic Treatment, and Behavioral Responses to Herding Efforts of a Cow-Calf Pair of Humpback Whales (Megaptera novaeangliae) in the Sacramento River Delta, California. Aquatic Mammals 32: 182-192.
66. Pettis HM, Rolland RM, Hamilton PK, Brault S, Knowlton AR, et al. (2004) Visual health assessment of North Atlantic right whales (Eubalaena glacialis) using photographs. Canadian Journal of Zoology 82: 8-19. (Pubitemid 38641570)
67. Scharschmidt TC, List K, Grice EA, Szabo R, Renaud G, et al. (2009) Matriptase-Deficient Mice Exhibit Ichthyotic Skin with a Selective Shift in Skin Microbiota. J Invest Dermatol 129: 2435-2442.