Advertisement

Microbial Ecology

, Volume 70, Issue 2, pp 534–544 | Cite as

Community Structure of Skin Microbiome of Gulf Killifish, Fundulus grandis, Is Driven by Seasonality and Not Exposure to Oiled Sediments in a Louisiana Salt Marsh

  • Andrea M. LarsenEmail author
  • Stephen A. Bullard
  • Matthew Womble
  • Covadonga R. Arias
Host Microbe Interactions

Abstract

Mucus of fish skin harbors complex bacterial communities that likely contribute to fish homeostasis. When the equilibrium between the host and its external bacterial symbionts is disrupted, bacterial diversity decreases while opportunistic pathogen prevalence increases, making the onset of pathogenic bacterial infection more likely. Because of that relationship, documenting temporal and spatial microbial community changes may be predictive of fish health status. The 2010 Deepwater Horizon oil spill was a potential stressor to the Gulf of Mexico’s coastal ecosystem. Ribosomal intergenic spacer analysis (RISA) and pyrosequencing were used to analyze the bacterial communities (microbiome) associated with the skin and mucus of Gulf killifish (Fundulus grandis) that were collected from oiled and non-oiled salt marsh sites in Barataria Bay, LA. Water samples and fin clips were collected to examine microbiome structure. The microbiome of Gulf killifish was significantly different from that of the surrounding water, mainly attributable to shifts in abundances of Cyanobacteria and Proteobacteria. The Gulf killifish’s microbiome was dominated by Gammaproteobacteria, specifically members of Pseudomonas. No significant difference was found between microbiomes of fish collected from oiled and non-oiled sites suggesting little impact of oil contamination on fish bacterial assemblages. Conversely, seasonality significantly influenced microbiome structure. Overall, the high similarity observed between the microbiomes of individual fish observed during this study posits that skin and mucus of Gulf killifish have a resilient core microbiome.

Keywords

Microbiome Fundulus grandis Oil spill Pyrosequencing 

Notes

Acknowledgments

We thank the Louisiana Department of Wildlife and Fisheries for facilitating access to collection sites; Carlos Ruiz (SFAAS), George Benz, and Eric Salmon (both from Middle Tennessee State University) for the help in collecting fish; and the Gulf of Mexico Research Initiative (SAB), National Science Foundation (SAB), and National Oceanic and Atmospheric Administration (PI, Arias) for the funding.

References

  1. 1.
    NOAA (2014) BP Oil Spill. http://www.gulfspillrestoration.noaa.gov/oil-spill. Accessed 28 Feb 2014
  2. 2.
    NOAA Fisheries Southeast Regional Office (2010) Deepwater Horizon/BP oil spill: size and percent coverage of fishing area closures due to oil spill. http://sero.nmfs.noaa.gov/deepwater_horizon/size_percent_closure/index.html. Accessed 28 Feb 2014
  3. 3.
    Innovative Emergency Management Inc (2010) A study of the economic impact of the Deepwater Horizon oil spill. Greater New Orleans Inc, New OrleansGoogle Scholar
  4. 4.
    McGill K (2011) Survey measure post-oil spill seafood attitudes. TheHuffingtonPost.com, Inc. http://www.huffingtonpost.com/huff-wires/20110131/la-gulf-oil-spill-seafood. Accessed 28 Feb 2014
  5. 5.
    Gundlach ER, Hayes MO (1978) Vulnerability of coastal environments to oil-spill impacts. Mar Technol Soc J 12:18–27Google Scholar
  6. 6.
    NOAA (2010) NOAA’s oil spill response: shorelines and coastal habitats in the Gulf of Mexico. http://www.noaa.gov/factsheets/new%20version/shorelines_coastalhabitat.pdf. Accessed 28 Feb 2014
  7. 7.
    Skinner MA, Courtenay SC, Parker WR, Curry RA (2005) Site fidelity of mummichogs (Fundulus heteroclitus) in an Atlantic Canadian estuary. Water Qual Res J Can 40:288–298Google Scholar
  8. 8.
    Griffin MPA, Valiela I (2001) Delta N-15 isotope studies of life history and trophic position of Fundulus heteroclitus and Menidia menidia. Mar Ecol Prog Ser 214:299–305CrossRefGoogle Scholar
  9. 9.
    Lotrich VA (1975) Summer home range and movements of Fundulus heteroclitus (Pisces-Cyprinodontidae) in a tidal creek. Ecology 56:191–198CrossRefGoogle Scholar
  10. 10.
    Teo SLH, Able KW (2003) Habitat use and movement of the mummichog (Fundulus heteroclitus) in a restored salt marsh. Estuaries 26:720–730CrossRefGoogle Scholar
  11. 11.
    Eisler R (1986) Use of Fundulus heteroclitus in pollution studies. Am Zool 26:283–288Google Scholar
  12. 12.
    Nacci DE, Champlin D, Jayaraman S (2010) Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuar Coasts 33:853–864. doi: 10.1007/s12237-009-9257-6 CrossRefGoogle Scholar
  13. 13.
    Ownby DR, Newman MC, Mulvey M, Vogelbein WK, Unger MA, Arzayus LF (2002) Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ Toxicol Chem 21:1897–1902PubMedCrossRefGoogle Scholar
  14. 14.
    Weis JS, Weis P (1989) Tolerance and stress in a polluted environment. Bioscience 39:89–95CrossRefGoogle Scholar
  15. 15.
    Weis JS, Weis P, Heber M, Vaidya S (1981) Methylmercury tolerance of killifish (Fundulus heteroclitus) embryos from a polluted vs non-polluted environment. Mar Biol 65:283–287CrossRefGoogle Scholar
  16. 16.
    Whitehead A, Triant DA, Champlin D, Nacci D (2010) Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Mol Ecol 19:5186–5203. doi: 10.1111/j.1365-294X.2010.04829.x PubMedCrossRefGoogle Scholar
  17. 17.
    Burnett KG, Bain LJ, Baldwin WS, Callard GV, Cohen S, Di Giulio RT, Evans DH, Gomez-Chiarri M, Hahn ME, Hoover CA, Karchner SI, Katoh F, MacLatchy DL, Marshall WS, Meyer JN, Nacci DE, Oleksiak MF, Rees BB, Singer TD, Stegeman JJ, Towle DW, Van Veld PA, Vogelbein WK, Whitehead A, Winn RN, Crawford DL (2007) Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp Biochem Phys D 2:257–286. doi: 10.1016/j.cbd.2007.09.001 Google Scholar
  18. 18.
    Crowe KM, Newton JC, Kaltenboeck B, Johnson C (2014) Oxidative stress response of Gulf killifish exposed to hydrocarbons from the Deepwater Horizon oil spill: potential implications for aquatic food resources. Environ Toxicol Chem 33:370–374. doi: 10.1002/etc.2427 PubMedCrossRefGoogle Scholar
  19. 19.
    Pilcher W, Miles S, Tang S, Mayer G, Whitehead A (2014) Genomic and genotoxic responses to controlled weathered-oil exposures confirm and extend field studies on impacts of the Deepwater Horizon oil spill on native killifish. PLoS One 9:e106351. doi: 10.1371/journal.pone.0106351 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Ramachandran SD, Sweezey MJ, Hodson PV, Boudreau M, Courtenay SC, Lee K, King T, Dixon JA (2006) Influence of salinity and fish species on PAH uptake from dispersed crude oil. Mar Pollut Bull 52:1182–1189. doi: 10.1016/j.marpolbul.2006.02.009 PubMedCrossRefGoogle Scholar
  21. 21.
    Ramachandran SD, Hodson PV, Khan CW, Lee K (2004) Oil dispersant increases PAH uptake by fish exposed to crude oil. Ecotoxicol Environ Saf 59:300–308. doi: 10.1016/j.ecoenv.2003.08.018 PubMedCrossRefGoogle Scholar
  22. 22.
    Giari L, Dezfuli BS, Lanzoni M, Castaldelli G (2012) The impact of an oil spill on organs of bream Abramis brama in the Po River. Ecotoxicol Environ Saf 77:18–27. doi: 10.1016/j.ecoenv.2011.10.014 PubMedCrossRefGoogle Scholar
  23. 23.
    Teal JM, Farrington JW, Burns KA, Stegeman JJ, Tripp BW, Woodin B, Phinney C (1992) The West Falmouth oil spill after 20 years—fate of fuel-oil compounds and effects on animals. Mar Pollut Bull 24:607–614CrossRefGoogle Scholar
  24. 24.
    Cipriano R (2011) Far from superficial: microbial diversity associated with the dermal mucus of fish. In: Cipriano R, Schelkunov I (eds) Health and diseases of aquatic organisms: bilateral perspectives. MSU Press, East Lansing, pp 156–167Google Scholar
  25. 25.
    Boutin S, Bernatchez L, Audet C, Derome N (2013) Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS One 8. doi:  10.1371/journal.pone.0084772
  26. 26.
    Llewellyn MS, Boutin S, Hoseinifar SH, Derome N (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol 5:1–17. doi: 10.3389/fmicb.2014.00207 CrossRefGoogle Scholar
  27. 27.
    Barron MG (2012) Ecological impacts of the Deepwater Horizon oil spill: implications for immunotoxicity. Toxicol Pathol 40:315–320. doi: 10.1177/0192623311428474 PubMedCrossRefGoogle Scholar
  28. 28.
    Ruiz CF (2013) Parasite component community of Gulf killifish, Fundulus grandis, in an oiled Louisiana saltmarsh. Auburn University, AuburnGoogle Scholar
  29. 29.
    Larsen A, Tao Z, Bullard SA, Arias CR (2013) Diversity of the skin microbiota of fishes: evidence for host species specificity. FEMS Microbiol Ecol 85:483–494. doi: 10.1111/1574-6941.12136 PubMedCrossRefGoogle Scholar
  30. 30.
    Mohammed HH, Arias CR (2014) Potassium permanganate disrupts the skin microbiota in channel catfish and increases susceptibility to Columnaris disease. 39th Annual Eastern Fish Health Workshop, Shepherdstown, West VirginiaGoogle Scholar
  31. 31.
    Lowrey LT (2011) The microbiome of rainbow trout (Oncorhynchus mykiss). University of New Mexico, AlbuquerqueGoogle Scholar
  32. 32.
    Wang WW, Zhou ZG, He SX, Liu YC, Cao YN, Shi PJ, Yao B, Ringo E (2010) Identification of the adherent microbiota on the gills and skin of poly-cultured gibel carp (Carassius auratus gibelio) and bluntnose black bream (Megalobrama amblycephala Yih). Aquac Res 41:e72–e83. doi: 10.1111/j.1365-2109.2009.02459.x CrossRefGoogle Scholar
  33. 33.
    Stevens JL, Olson JB (2013) Invasive lionfish harbor a different external bacterial community than native Bahamian fishes. Coral Reefs 32:1113–1121. doi: 10.1007/s00338-013-1072-7 CrossRefGoogle Scholar
  34. 34.
    Jensen S, Ovreas L, Bergh O, Torsvik V (2004) Phylogenetic analysis of bacterial communities associated with larvae of the Atlantic halibut propose succession from a uniform normal flora. Syst Appl Microbiol 27:728–736. doi: 10.1078/0723202042369929 PubMedCrossRefGoogle Scholar
  35. 35.
    Smith CJ, Danilowicz BS, Meijer WG (2007) Characterization of the bacterial community associated with the surface and mucus layer of whiting (Merlangius merlangus). FEMS Microbiol Ecol 62:90–97. doi: 10.1111/j.1574-6941.2007.00369.x PubMedCrossRefGoogle Scholar
  36. 36.
    Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147–6156. doi: 10.1128/Aem. 70.10.6147-6156.2004 PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Boutin S, Sauvage C, Bernatchez L, Audet C, Derome N (2014) Inter individual variations of the fish skin microbiota: host genetics basis of mutualism? PLoS One 9:e102649. doi: 10.1371/journal.pone.0102649 PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Rossello-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67. doi: 10.1016/S0168-6445(00)00040-1 PubMedCrossRefGoogle Scholar
  39. 39.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. doi: 10.1128/Aem. 03006-05 PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Arias CR, Abernathy JW, Liu Z (2006) Combined use of 16S ribosomal DNA and automated ribosomal intergenic spacer analysis to study the bacterial community in catfish ponds. Lett Appl Microbiol 43:287–292. doi: 10.1111/j.1472-765X.2006.01955.x PubMedCrossRefGoogle Scholar
  41. 41.
    Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636PubMedCentralPubMedGoogle Scholar
  42. 42.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi: 10.1128/Aem. 01541-09 PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial, Plymouth, UKGoogle Scholar
  44. 44.
    Georgala DL (1958) The bacterial flora of the skin of North Sea cod. J Gen Microbiol 18:84–91PubMedCrossRefGoogle Scholar
  45. 45.
    Wilson B, Danilowicz BS, Meijer WG (2008) The diversity of bacterial communities associated with Atlantic cod Gadus morhua. Microb Ecol 55:425–434. doi: 10.1007/s00248-007-9288-0 PubMedCrossRefGoogle Scholar
  46. 46.
    Colwell RR, Liston J (1962) Bacterial flora of seven species of fish collected at Rongelap and Eniwetok atolls. Pac Sci 16:264–270Google Scholar
  47. 47.
    Austin B (2006) The bacterial microflora of fish, revised. Sci World J 6:931–945. doi: 10.1100/Tsw.2006.181 CrossRefGoogle Scholar
  48. 48.
    Horsley RW (1973) Bacterial flora of Atlantic salmon (Salmo-Salar L) in relation to its environment. J Appl Bacteriol 36:377–386PubMedCrossRefGoogle Scholar
  49. 49.
    Arias CR, Koenders K, Larsen AM (2013) Predominant bacteria associated with red snapper from the northern Gulf of Mexico. J Aquat Anim Health 25:281–289PubMedCrossRefGoogle Scholar
  50. 50.
    Givens CE (2012) A fish tale: comparison of the gut microbiome of 15 fish species and the influence of diet and temperature on its composition. University of Georgia, AthensGoogle Scholar
  51. 51.
    Kurnia A, Satoh S, Hanzawa S (2010) Effect of Paracoccus sp. and their genetically modified on skin coloration of red sea bream. HAYATI J Biosci 17:79–84CrossRefGoogle Scholar
  52. 52.
    Satoh S, Hanzawa S, Kuramoto D, Kurnia A (2007) Effect of different astaxanthin sources on skin pigmentation of red sea bream (Pagrus major). Aquac Sci 55:441–447Google Scholar
  53. 53.
    Liu Y, Xie QY, Hong K, Li L, Zhao YM, Tang YL, An JY, Zhu PP, Xu CH (2013) Paracoccus siganidrum sp nov., isolated from fish gastrointestinal tract. Anton Leeuw Int J G 103:1133–1139. doi: 10.1007/s10482-013-9894-4 CrossRefGoogle Scholar
  54. 54.
    Nalin R, Simonet P, Vogel TM, Normand P (1999) Rhodanobacter lindaniclasticus gen. nov., sp, nov., a lindane-degrading bacterium. Int J Syst Bacteriol 49:19–23PubMedCrossRefGoogle Scholar
  55. 55.
    Lv X, Yu J, Fu Y, Ma B, Qu F, Ning K, Wu H (2014) A meta-analysis of the bacterial and archaeal diversity observed in wetland soils. Sci World J 2014:437684. doi: 10.1155/2014/437684 Google Scholar
  56. 56.
    Li X, Yu Y, Feng W, Yan Q, Gong Y (2012) Host species as a strong determinant of the intestinal microbiota of fish larvae. J Microbiol 50:29–37. doi: 10.1007/s12275-012-1340-1 PubMedCrossRefGoogle Scholar
  57. 57.
    Larsen AM, Mohammed HH, Arias CR (2014) Characterization of the gut microbiota of three commercially valuable warmwater fish species. J Appl Microbiol 116:1396–1404. doi: 10.1111/jam.12475 PubMedCrossRefGoogle Scholar
  58. 58.
    Hartviksen M, Vecino JLG, Ringo E, Bakke AM, Wadsworth S, Krogdahl A, Ruohonen K, Kettunen A (2014) Alternative dietary protein sources for Atlantic salmon (Salmo salar L.) effect on intestinal microbiota, intestinal and liver histology and growth. Aquacult Nutr 20:381–398. doi: 10.1111/anu.12087 CrossRefGoogle Scholar
  59. 59.
    Mengxin X, Zhanbui H, Yanmei Q, Bin L (2014) Enhancing the culturability of bacteria from the gastrointestinal tract of farmed adult turbot Scophthalmus maximus. Chin J Oceanol Limnol 32:315–325. doi: 10.1007/s00343-014-3099-1 Google Scholar
  60. 60.
    Roberts RJ, Bullock AM (1980) The skin surface ecosystem of teleost fishes. Proc R Soc Edinb B 79:87–91Google Scholar
  61. 61.
    Dubansky B, Whitehead A, Miller JT, Rice CD, Galvez F (2013) Multitissue molecular, genomic, and developmental effects of the Deepwater Horizon oil spill on resident Gulf killifish (Fundulus grandis). Environ Sci Technol 47:5074–5082. doi: 10.1021/Es400458p PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Whitehead A, Dubansky B, Bodinier C, Garcia TI, Miles S, Pilley C, Raghunathan V, Roach JL, Walker N, Walter RB, Rice CD, Galvez F (2012) Genomic and physiological footprint of the Deepwater Horizon oil spill on resident marsh fishes. Proc Natl Acad Sci U S A 109:20298–20302. doi: 10.1073/pnas.1109545108 PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Ali AO, Hohn C, Allen PJ, Ford L, Dail MB, Pruett S, Petrie-Hanson L (2014) The effects of oil exposure on peripheral blood leukocytes and splenic melano-macrophage centers of Gulf of Mexico fishes. Mar Pollut Bull 79:87–93PubMedCrossRefGoogle Scholar
  64. 64.
    Garcia TI, Shen YJ, Crawford D, Oleksiak MF, Whitehead A, Walter RB (2012) RNA-Seq reveals complex genetic response to deepwater horizon oil release in Fundulus grandis. BMC Genomics 13:474. doi: 10.1186/1471-2164-13-474 PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363. doi: 10.1038/ismej.2007.112 PubMedCrossRefGoogle Scholar
  66. 66.
    Gil-Agudelo DL, Myers C, Smith GW, Kim K (2006) Changes in the microbial communities associated with Gorgonia ventalina during aspergillosis infection. Dis Aquat Organ 69:89–94PubMedCrossRefGoogle Scholar
  67. 67.
    Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68:2214–2228. doi: 10.1128/Aem. 68.5.2214-2228.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Arboleda M, Reichardt WG (2009) Epizoic communities of prokaryotes on healthy and diseased scleractinian corals in Lingayen Gulf, Philippines. Microb Ecol 57:117–128. doi: 10.1007/s00248-008-9400-0 PubMedCrossRefGoogle Scholar
  69. 69.
    Whitehead A, Crawford DL (2006) Neutral and adaptive variation in gene expression. Proc Natl Acad Sci U S A 103:5425–5430. doi: 10.1073/pnas.0507648103 PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Whitehead A, Crawford DL (2005) Variation in tissue-specific gene expression among natural populations. Genome Biol 6. doi: 10.1186/Gb-2005-6-2-R13
  71. 71.
    Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nat Genet 32:261–266. doi: 10.1038/Ng983 PubMedCrossRefGoogle Scholar
  72. 72.
    Oleksiak MF, Roach JL, Crawford DL (2005) Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus. Nat Genet 37:67–72. doi: 10.1038/Ng1483 PubMedCentralPubMedGoogle Scholar
  73. 73.
    Nelson TR, Sutton D, DeVries DR (2014) Summer movements of the Gulf killifish (Fundulus grandis) in a Northern Gulf of Mexico salt marsh. Estuar Coast: 1–6. doi:  10.1007/s12237-013-9762-5
  74. 74.
    Nelson TR (2014) Fundulus grandis otolith microchemistry as a metric of estuarine discrimination and environmental conditions in the northern Gulf of Mexico. Auburn University, AuburnGoogle Scholar
  75. 75.
    Horsley RW (1977) Review of bacterial flora of teleosts and elasmobranchs, including methods for its analysis. J Fish Biol 10:529–553CrossRefGoogle Scholar
  76. 76.
    Le Nguyen DD, Ngoc HH, Dijoux D, Loiseau G, Montet D (2008) Determination of fish origin by using 16S rDNA fingerprinting of bacterial communities by PCR-DGGE: an application on Pangasius fish from Viet Nam. Food Control 19:454–460. doi: 10.1016/j.foodcont.2007.05.006 CrossRefGoogle Scholar
  77. 77.
    Naviner M, Giraud E, Le Bris H, Armand F, Mangion C, Ganiere J-P (2006) Seasonal variability of intestinal microbiota in rainbow trout (Oncorhynchus mykiss), with a particular attention to Aeromonas spp. as candidate indicator of antimicrobial resistance. Rev Med Vet 157:599–604Google Scholar
  78. 78.
    Tatsadjieu NL, Maiwore J, Hadjia MB, Loiseau G, Montet D, Mbofung CMF (2010) Study of the microbial diversity of Oreochromis niloticus of three lakes of Cameroon by PCR-DGGE: application to the determination of the geographical origin. Food Control 21:673–678CrossRefGoogle Scholar
  79. 79.
    Logan NA (1989) Numerical taxonomy of violet-pigmented, Gram-negative bacteria and description of Iodobacter fluviatile gen. nov., comb. nov. Int J Syst Bacteriol 39:450–456CrossRefGoogle Scholar
  80. 80.
    Alonso-Saez L, Zeder M, Harding T, Pernthaler J, Lovejoy C, Bertilsson S, Pedros-Alio C (2014) Winter bloom of a rare betaproteobacterium in the Arctic Ocean. Front Microbiol. doi: 10.3389/fmicb.2014.00425 PubMedCentralPubMedGoogle Scholar
  81. 81.
    Hatje E, Neuman C, Stevenson H, Bowman JP, Katouli M (2014) Population dynamics of Vibrio and Pseudomonas species isolated from farmed Tasmanian Atlantic salmon (Salmo salar L.): a seasonal study. Microb Ecol 68:679–687. doi: 10.1007/s00248-014-0462-x PubMedCrossRefGoogle Scholar
  82. 82.
    Tao Z, Larsen AM, Bullard SA, Wright AC, Arias CR (2012) Prevalence and population structure of Vibrio vulnificus on fishes from the Northern Gulf of Mexico. Appl Environ Microbiol 78:7611–7618. doi: 10.1128/AEM. 01646-12 PubMedCentralPubMedCrossRefGoogle Scholar
  83. 83.
    NOAA National Data Buoy Center (2011) Station GISL1—Grand Isle, LA. http://www.ndbc.noaa.gov/station_page.php?station=gisl1. Accessed 2 April 2014

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Andrea M. Larsen
    • 1
    • 2
    Email author
  • Stephen A. Bullard
    • 1
  • Matthew Womble
    • 1
  • Covadonga R. Arias
    • 1
  1. 1.School of Fisheries, Aquaculture, and Aquatic SciencesAuburn UniversityAuburnUSA
  2. 2.Mote Marine LaboratorySarasotaUSA

Personalised recommendations