Aquatic Sciences

, Volume 77, Issue 3, pp 481–497 | Cite as

Declining diversity of egg-associated bacteria during development of naturally spawned whitefish embryos (Coregonus spp.)

  • Laetitia G. E. Wilkins
  • Aude Rogivue
  • Luca Fumagalli
  • Claus Wedekind
Research Article


Fish eggs are associated with microbes, whose roles range from mutualism to parasitism. Recent laboratory experiments have shown that the taxonomic composition of associated microbial communities on the egg influences embryonic development. Host genetics also plays an important role in determining the consequences for embryonic growth and survival in this interaction. Moreover, it has been found that the importance of host genetics increases during embryogenesis. These findings suggest that during embryogenesis, the host increasingly influences the composition of its associated microbial community. However, little is known about the composition of microbial communities associated with naturally spawned eggs in the wild. We sampled fertilized whitefish eggs (Coregonus spp.) of different developmental stages from six sub-Alpine lakes and used a universal primer pair and 454 pyrosequencing in order to describe the taxonomic composition of egg-associated bacterial communities. We found bacterial communities on early embryos to be very diverse and to resemble the bacterial composition of the surrounding water environment. The bacterial communities on late embryos were significantly less diverse than on early embryos and displayed a clear shift in taxonomic composition that corresponded poorly with the bacterial composition of the surrounding water environment. The main bacterial components on whitefish eggs in this study were Proteobacteria, Actinobacteria, and Firmicutes, while the five most common families were Leuconostocaceae, Streptococcaceae, Comamonadaceae, Oxalobacteraceae and Moraxellaceae. Their putative relationships with the host are discussed. We conclude that natural symbiotic bacterial communities become more specialized during embryogenesis because of specific interactions with their embryo host.


Bacterial community Coregonus Metagenomics Microbiome Salmonids Whitefish 



The fieldwork was permitted by the fisheries authorities of the cantons of Berne, Lucerne, and Vaud. We thank Philippe Amiet, Joachim Guthruf, Frédéric Hofmann, Christoph Küng, Joseph Muggli, Rudolph Müller, Patrick Porchet, Rolf Schneider, and Gérard Zürcher for permissions, organizational support, or help in finding the spawning places and collecting the eggs. Cathérine Berney, Gregory Brazzola, Emily Clark, Hélène Collin, Lucas Marques da Cunha, Miguel dos Santos, Simon Gingins, Marianne Johner, Catalina Luca, Yves Poirier, Manuel Pompini, Thorsten Reusch, Adin Ross-Gillespie, Vladimir Sentchilo, Rike Stelkens, Pierre Taberlet, Anshu Uppal, Jan Roelof van der Meer, Beat von Siebenthal, Donny Wilkins, Fardo Witsenburg, and Erika Yashiro are thanked for assistance or discussion, and the Swiss National Science Foundation for financial support. We also thank Stuart Findlay and two anonymous reviewers for comments on the manuscript. L. Wilkins was supported by a fellowship in Life Sciences from the Faculty of Biology and Medicine of the University of Lausanne.

Supplementary material

27_2015_392_MOESM1_ESM.pdf (955 kb)
Supplementary material 1 (PDF 954 kb)


  1. Allison MJ, Dawson KA, Mayberry WR, Foss JG (1985) Oxalobacter formigenes gen. nov., sp. nov., oxalate degrading anaerobes that inhabit the gastrointestinal tract. Arch Microbiol 141(1):1–7PubMedGoogle Scholar
  2. Amann R, Ludwig W (2000) Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol Rev 24(5):555–565PubMedGoogle Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26(1):32–46Google Scholar
  4. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1):245–253PubMedGoogle Scholar
  5. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84(2):511–525Google Scholar
  6. Arahal DR, Sanchez E, Macian MC, Garay E (2008) Value of recN sequences for species identification and as a phylogenetic marker within the family ‘Leuconostocaceae’. Int Microbiol 11(1):33–39PubMedGoogle Scholar
  7. Austin B, Austin DA (2007) Bacterial fish pathogens: diseases of farmed and wild fish, 5th edn. Springer, LondonGoogle Scholar
  8. Aykanat T, Heath JW, Dixon B, Heath DD (2012) Additive, non-additive and maternal effects of cytokine transcription in response to immunostimulation with Vibrio vaccine in Chinook salmon (Oncorhynchus tshawytscha). Immunogenetics 64(9):691–703PubMedGoogle Scholar
  9. Behar A, Yuval B, Jurkevitch E (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol 14(9):2637–2643PubMedGoogle Scholar
  10. Berry D, Ben Mahfoudh K, Wagner M, Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microb 77(21):7846–7849Google Scholar
  11. Boutin S, Sevellec M, Pavey SA, Bernatchez L, Derome N (2012) A fast, highly sensitive double-nested PCR-based method to screen fish immunobiomes. Mol Ecol Resour 12(6):1027–1039PubMedGoogle Scholar
  12. Brivio MF, Bassi R, Cotelli F (1991) Identification and characterization of the major components of the Oncorhynchus mykiss egg chorion. Mol Reprod Dev 28(1):85–93PubMedGoogle Scholar
  13. Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341(6146):667–669PubMedGoogle Scholar
  14. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108(34):14288–14293PubMedCentralPubMedGoogle Scholar
  15. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2):266–267PubMedCentralPubMedGoogle Scholar
  16. 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, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336PubMedCentralPubMedGoogle Scholar
  17. Casadevall A, Pirofski LA (1999) Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 67(8):3703–3713PubMedCentralPubMedGoogle Scholar
  18. Casadevall A, Pirofski LA (2000) Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun 68(12):6511–6518PubMedCentralPubMedGoogle Scholar
  19. Clark E, Wedekind C (2011) Additive genetic effects on embryo viability in a whitefish (Salmonidae) influenced by the water mould Saprolegnia ferax. J Bacteriol Parasitol 10:2–6Google Scholar
  20. Clark ES, Wilkins LGE, Wedekind C (2013) MHC class I expression dependent on bacterial infection and parental factors in whitefish embryos (Salmonidae). Mol Ecol 22(20):5256–5269PubMedGoogle Scholar
  21. Clark ES, Pompini M, Marques da Cunha L, Wedekind C (2014) Maternal and paternal contributions to pathogen resistance dependent on development stage in a whitefish. Funct Ecol 28:714–723Google Scholar
  22. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The ribosomal database project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33(Database issue):D294–D296PubMedCentralPubMedGoogle Scholar
  23. Cordero OX, Wildschutte H, Kirkup B, Proehl S, Ngo L, Hussain F, Le Roux F, Mincer T, Polz MF (2012) Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 337(6099):1228–1231PubMedGoogle Scholar
  24. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326(5960):1694–1697PubMedCentralPubMedGoogle Scholar
  25. Coulon F, McKew BA, Osborn AM, McGenity TJ, Timmis KN (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol 9(1):177–186PubMedGoogle Scholar
  26. Crete-Lafreniere A, Weir LK, Bernatchez L (2012) Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling. PLoS One 7(10):e46662PubMedCentralPubMedGoogle Scholar
  27. Denton M, Kerr KG (1998) Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 11(1):57–80PubMedCentralPubMedGoogle Scholar
  28. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92PubMedGoogle Scholar
  29. Douglas AE (1994) Symbiotic interactions. Oxford University Press, OxfordGoogle Scholar
  30. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461PubMedGoogle Scholar
  31. Ehrich S, Behrens D, Lebedeva E, Ludwig W, Bock E (1995) A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch Microbiol 164(1):16–23PubMedGoogle Scholar
  32. Eissa NME, Abou El-Ghiet EN, Shaheen AA, Abbas A (2010) Characterization of Pseudomonad species isolated form Tilapia “Oreochromis niloticus” in Qaroun and Wadi-El-Rayan Lakes. Egypt. Global Veterinaria 5(2):116–121Google Scholar
  33. Ellis AE (2001) Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol 25(8–9):827–839PubMedGoogle Scholar
  34. Evans ML, Neff BD (2009) Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol 18(22):4716–4729PubMedGoogle Scholar
  35. Evans ML, Neff BD, Heath DD (2010) MHC-mediated local adaptation in reciprocally translocated Chinook salmon. Conserv Genet 11(6):2333–2342Google Scholar
  36. Evans ML, Praebel K, Peruzzi S, Bernatchez L (2012) Parallelism in the oxygen transport system of the lake whitefish: the role of physiological divergence in ecological speciation. Mol Ecol 21(16):4038–4050PubMedGoogle Scholar
  37. Fierer N, Lauber CL, Zhou N, McDonald D, Costello EK, Knight R (2010) Forensic identification using skin bacterial communities. Proc Natl Acad Sci USA 107(14):6477–6481PubMedCentralPubMedGoogle Scholar
  38. Finn RN (2007) The physiology and toxicology of salmonid eggs and larvae in relation to water quality criteria. Aquat Toxicol 81(4):337–354PubMedGoogle Scholar
  39. Fodelianakis S, Papageorgiou N, Pitta P, Kasapidis P, Karakassis I, Ladoukakis ED (2014) The Pattern of change in the abundances of specific bacterioplankton groups is consistent across different nutrient-enriched habitats in Crete. Appl Environ Microb 80(13):3784–3792Google Scholar
  40. Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11(8):e1001631PubMedCentralPubMedGoogle Scholar
  41. Gattuso JP, Peduzzi S, Pizay MD, Tonolla M (2002) Changes in freshwater bacterial community composition during measurements of microbial and community respiration. J Plankton Res 24(11):1197–1206Google Scholar
  42. Gilbert JA, Field D, Swift P, Thomas S, Cummings D, Temperton B, Weynberg K, Huse S, Hughes M, Joint I, Somerfield PJ, Muhling M (2010) The taxonomic and functional diversity of microbes at a temperate coastal site: a ‘multi-omic’ study of seasonal and diel temporal variation. PLoS One 5(11):e15545PubMedCentralPubMedGoogle Scholar
  43. Git A, Dvinge H, Salmon-Divon M, Osborne M, Kutter C, Hadfield J, Bertone P, Caldas C (2010) Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. RNA 16(5):991–1006PubMedCentralPubMedGoogle Scholar
  44. Gotelli NJ, Chao A (2013) Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. In: Levin SA (ed) Encyclopedia of Biodiversity, vol 5, 2nd edn. Academic Press, Waltham, pp 195–211Google Scholar
  45. Hahn MW, Lang E, Brandt U, Lünsdorf H, Wu QL, Stackebrandt E (2010) Polynucleobacter cosmopolitanus sp. nov., free-living planktonic bacteria inhabiting freshwater lakes and rivers. Int J Syst Evol Microbiol 60:166–173PubMedCentralPubMedGoogle Scholar
  46. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5(3):235–237PubMedCentralPubMedGoogle Scholar
  47. Hanif A, Bakopoulos V, Dimitriadis GJ (2004) Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae. Fish Shellfish Immun 17(5):411–435Google Scholar
  48. Hari RE, Livingstone DM, Siber R, Burkhardt-Holm P, Guttinger H (2006) Consequences of climatic change for water temperature and brown trout populations in Alpine rivers and streams. Global Change Biol 12(1):10–26Google Scholar
  49. Hecht BC, Thrower FP, Hale MC, Miller MR, Nichols KM (2012) Genetic architecture of migration-related traits in rainbow and steelhead trout, Oncorhynchus mykiss. G3-Genes Genomes Genet 2(9):1113–1127Google Scholar
  50. Henry EA, Devereux R, Maki JS, Gilmour CC, Woese CR, Mandelco L, Schauder R, Remsen CC, Mitchell R (1994) Characterization of a new thermophilic sulfate-reducing bacterium—Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov., its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the bacterial domain. Arch Microbiol 161(1):62–69PubMedGoogle Scholar
  51. Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43(1):1–11PubMedGoogle Scholar
  52. Hollander M, Wolfe DA (1973) Nonparametric statistical methods, 2nd edn. Wiley, New YorkGoogle Scholar
  53. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292(5519):1115–1118PubMedGoogle Scholar
  54. Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307PubMedGoogle Scholar
  55. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2002) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microb 68(1):448Google Scholar
  56. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4(11):e1000255PubMedCentralPubMedGoogle Scholar
  57. Hutchings JA, Morris DW (1985) The influence of phylogeny, size and behavior on patterns of covariation in salmonid life histories. Oikos 45(1):118–124Google Scholar
  58. Ivanova EP, Flavier S, Christen R (2004) Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Montellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov and Psychromonadaceae fam. nov. Int J Syst Evol Microbiol 54:1773–1788PubMedGoogle Scholar
  59. Jacob A, Evanno G, von Siebenthal BA, Grossen C, Wedekind C (2010) Effects of different mating scenarios on embryo viability in brown trout. Mol Ecol 19(23):5296–5307PubMedGoogle Scholar
  60. Johnson DR, Goldschmidt F, Lilja EE, Ackermann M (2012) Metabolic specialization and the assembly of microbial communities. ISME J 6(11):1985–1991PubMedCentralPubMedGoogle Scholar
  61. Joseph SJ, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH (2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol 69(12):7210–7215PubMedCentralPubMedGoogle Scholar
  62. Jung A, Jung-Schroers V (2011) Detection of Deefgea chitinilytica in freshwater ornamental fish. Lett Appl Microbiol 52(5):497–500PubMedGoogle Scholar
  63. Junier P, Kim OS, Hadas O, Imhoff JF, Witzel KP (2008) Evaluation of PCR primer selectivity and phylogenetic specificity by using amplification of 16S rRNA genes from betaproteobacterial ammonia-oxidizing bacteria in environmental samples. Appl Environ Microbiol 74(16):5231–5236PubMedCentralPubMedGoogle Scholar
  64. Kim S, Gong G, Park TH, Um Y (2013) Asticcacaulis solisilvae sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 63:3829–3834PubMedGoogle Scholar
  65. Kojima H, Fukui M (2011) Sulfuritalea hydrogenivorans gen. nov., sp. nov., a facultative autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 61:1651–1655PubMedGoogle Scholar
  66. Kottelat M, Freyhof J (2007) Handbook of European Freshwater Fishes. Kottelat/Freyhof, Cornol/BerlinGoogle Scholar
  67. Lan YM, Wang Q, Cole JR, Rosen GL (2012) Using the RDP classifier to predict taxonomic novelty and reduce the search space for finding novel organisms. PLoS One 7(3):e3249Google Scholar
  68. 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(3):483–494PubMedGoogle Scholar
  69. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(15):5111–5120PubMedCentralPubMedGoogle Scholar
  70. Lee KB, Liu CT, Anzai Y, Kim H, Aonol T, Oyaizu H (2005) The hierarchical system of the ‘Alphaproteobacteria’: description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov., and Erythrobacteraceae fam. nov. Int J Syst Evol Microbiol 55:1907–1919PubMedGoogle Scholar
  71. Lee CM, Weon HY, Kim YJ, Son JA, Yoon SH, Koo BS, Kwon SW (2012) Aquitalea denitrificans sp. nov., isolated from a Korean wetland. Int J Syst Evol Micrbiol 62:259Google Scholar
  72. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69(1):1–24Google Scholar
  73. Leisner JJ, Laursen BG, Prevost H, Drider D, Dalgaard P (2007) Carnobacterium: positive and negative effects in the environment and in foods. FEMS Microbiol Rev 31(5):592–613PubMedCentralPubMedGoogle Scholar
  74. 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(5883):1647–1651PubMedCentralPubMedGoogle Scholar
  75. Lighten J, van Oosterhout C, Paterson IG, McMullan M, Bentzen P (2014) Ultra-deep Illumina sequencing accurately identifies MHC class IIb alleles and provides evidence for copy number variation in the guppy (Poecilia reticulata). Mol Ecol Resour (in press)Google Scholar
  76. Løvoll M, Kilvik T, Boshra H, Bogwald J, Sunyer JO, Dalmo RA (2006) Maternal transfer of complement components C3-1, C3-3, C3-4, C4, C5, C7, Bf, and Df to offspring in rainbow trout (Oncorhynchus mykiss). Immunogenetics 58(2–3):168–179PubMedGoogle Scholar
  77. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microb 71(12):8228–8235Google Scholar
  78. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104(27):11436–11440PubMedCentralPubMedGoogle Scholar
  79. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5(2):169–172PubMedCentralPubMedGoogle Scholar
  80. Luczynski M, Kirklewska A (1984) Dependence of Coregonus albula embryogenesis rate on the incubation temperature. Aquaculture 42(1):43–55Google Scholar
  81. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Inc., SunderlandGoogle Scholar
  82. Madigan MT, Martinko JM, Stahl D, Clark DP (2010) Brock biology of microorganisms, 13th edn. Benjamin Cummings, San FranciscoGoogle Scholar
  83. Maher M, Palmer R, Gannon F, Smith T (1995) Relationship of a novel bacterial fish pathogen to Streptobacillus moniliformis and the Fusobacteria group, based on 16s Ribosomal RNA analysis. Syst Appl Microbiol 18(1):79–84Google Scholar
  84. Maret TR, Robinson CT, Minshall GW (1997) Fish assemblages and environmental correlates in least-disturbed streams of the upper Snake River basin. Trans Am Fish Soc 126(2):200–216Google Scholar
  85. Martin G, Guggiari M, Bravo D, Zopfi J, Cailleau G, Aragno M, Job D, Verrecchia E, Junier P (2012) Fungi, bacteria and soil pH: the oxalate-carbonate pathway as a model for metabolic interaction. Environ Microbiol 14(11):2960–2970PubMedGoogle Scholar
  86. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82(1):290–297Google Scholar
  87. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618PubMedCentralPubMedGoogle Scholar
  88. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217PubMedCentralPubMedGoogle Scholar
  89. Milligan-Myhre K, Charette JR, Phennicie RT, Stephens WZ, Rawls JF, Guillemin K, Kim CH (2011) Study of host-microbe interactions in zebrafish. Method Cell Biol 105:87–116Google Scholar
  90. Mouchet MA, Bouvier C, Bouvier T, Troussellier M, Escalas A, Mouillot D (2012) Genetic difference but functional similarity among fish gut bacterial communities through molecular and biochemical fingerprints. FEMS Microbiol Ecol 79(3):568–580PubMedGoogle Scholar
  91. Müller R, Stadelmann P (2004) Fish habitat requirements as the basis for rehabilitation of eutrophic lakes by oxygenation. Fish Manag Ecol 11(3–4):251–260Google Scholar
  92. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267PubMedGoogle Scholar
  93. Nusslé S, Bornand CN, Wedekind C (2009) Fishery-induced selection on an Alpine whitefish: quantifying genetic and environmental effects on individual growth rate. Evol Appl 2:200–208PubMedCentralPubMedGoogle Scholar
  94. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stenvens MHH, Wagner H (2013) vegan: Community Ecology Package. R package version 2.0-8Google Scholar
  95. Ong SH, Kukkillaya VU, Wilm A, Lay C, Ho EXP, Low L, Hibberd ML, Nagarajan N (2013) Species identification and profiling of complex microbial communities using shotgun Illumina sequencing of 16S rRNA amplicon sequences. PLoS One 8(4):e60811PubMedCentralPubMedGoogle Scholar
  96. Pantoja-Feliciano IG, Clemente JC, Costello EK, Perez ME, Blaser MJ, Knight R, Dominguez-Bello MG (2013) Biphasic assembly of the murine intestinal microbiota during early development. ISME J 7(6):1112–1115PubMedCentralPubMedGoogle Scholar
  97. Patureau D, Bernet N, Bouchez T, Dabert P, Delgenes JP, Moletta R (1998) Biological nitrogen removal in a single aerobic reactor by association of a nitrifying ecosystem to an aerobic denitrifier, Microvirgula aerodenitrificans. J Mol Catal B-Enzym 5(1–4):435–439Google Scholar
  98. Pavey SA, Sevellec M, Adam W, Normandeau E, Lamaze FC, Gagnaire PA, Filteau M, Hebert FO, Maaroufi H, Bernatchez L (2013) Nonparallelism in MHC II diversity accompanies nonparallelism in pathogen infection of lake whitefish (Coregonus clupeaformis) species pairs as revealed by next-generation sequencing. Mol Ecol 22(14):3833–3849PubMedGoogle Scholar
  99. Pitcher TE, Neff BD (2006) MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon. Mol Ecol 15(9):2357–2365PubMedGoogle Scholar
  100. Price MN, Dehal PS, Arkin AP (2008) FastBLAST: homology relationships for millions of proteins. PLoS One 3(10):e3589PubMedCentralPubMedGoogle Scholar
  101. Qi WH, Nong G, Preston JF, Ben-Ami F, Ebert D (2009) Comparative metagenomics of Daphnia symbionts. BMC Genomics 10(1):172Google Scholar
  102. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA 108:4680–4687PubMedCentralPubMedGoogle Scholar
  103. Rendueles O, Ferrieres L, Fretaud M, Begaud E, Herbomel P, Levraud JP, Ghigo JM (2012) A new zebrafish model of oro-intestinal pathogen colonization reveals a key role for adhesion in protection by probiotic bacteria. PLoS Pathog 8(7):e1002815PubMedCentralPubMedGoogle Scholar
  104. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C, Keller H, Lambert C, Evans KJ, Goesmann A, Meyer F, Sockett RE, Schuster SC (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303(5658):689–692PubMedGoogle Scholar
  105. Romero J, Navarrete P (2006) 16S rDNA-based analysis of dominant bacterial populations associated with early life stages of coho salmon (Oncorhynchus kisutch). Microb Ecol 51(4):422–430PubMedGoogle Scholar
  106. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5(5):355–362PubMedGoogle Scholar
  107. Roychoudhury AN, Cowan D, Porter D, Valverde A (2013) Dissimilatory sulphate reduction in hypersaline coastal pans: an integrated microbiological and geochemical study. Geobiology 11(3):224–233PubMedGoogle Scholar
  108. Salonen A, Nikkila J, Jalanka-Tuovinen J, Immonen O, Rajilic-Stojanovic M, Kekkonen RA, Palva A, de Vos WM (2010) Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Meth 81(2):127–134Google Scholar
  109. Schauer M, Kamenik C, Hahn MW (2005) Ecological differentiation within a cosmopolitan group of planktonic freshwater bacteria (SOL cluster, Saprospiraceae, Bacteroidetes). Appl Environ Microb 71(10):5900–5907Google Scholar
  110. Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6(8):229PubMedCentralPubMedGoogle Scholar
  111. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6(12):e27310PubMedCentralPubMedGoogle Scholar
  112. Schloss PD, Schubert AM, Zackular JP, Iverson KD, Young VB, Petrosino JF (2012) Stabilization of the murine gut microbiome following weaning. Gut Microbes 3(4):383–393PubMedCentralPubMedGoogle Scholar
  113. Sevellec M, Pavey S, Boutin S, Filteau M, Derome N, Bernatchez L (2014) Microbiome investigation in the ecological speciation context of lake whitefish (Coregonus clupeaformis) using next generation sequencing. J Evol Biol 27(6):1029–1046PubMedGoogle Scholar
  114. Shade A, Read JS, Youngblut ND, Fierer N, Knight R, Kratz TK, Lottig NR, Roden EE, Stanley EH, Stombaugh J, Whitaker RJ, Wu CH, McMahon KD (2012) Lake microbial communities are resilient after a whole-ecosystem disturbance. ISME J 6(12):2153–2167PubMedCentralPubMedGoogle Scholar
  115. Shi WB, Syrenne R, Sun JZ, Yuan JS (2010) Molecular approaches to study the insect gut symbiotic microbiota at the ‘omics’ age. Insect Sci 17(3):199–219Google Scholar
  116. Shin YK, Hiraishi A, Sugiyama J (1993) Molecular systematics of the genus Zoogloea and emendation of the genus. Int J Syst Bacteriol 43(4):826–831PubMedGoogle Scholar
  117. Simek K, Kasalicky V, Jezbera J, Jezberova J, Hejzlar J, Hahn MW (2010) Broad habitat range of the phylogenetically narrow R-BT065 cluster, representing a core group of the Betaproteobacterial genus Limnohabitans. Appl Environ Microb 76(3):631–639Google Scholar
  118. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Google Scholar
  119. Treasurer JW, Cochrane E, Grant A (2005) Surface disinfection of cod Gadus morhua and haddock Melanogrammus aeglefinus eggs with bronopol. Aquaculture 250(1–2):27–35Google Scholar
  120. Urakami T, Oyanagi H, Araki H, Suzuki K-I, Komagata K (1990) Recharacterization and emended description of the genus Mycoplana and description of two new species, Mycoplana ramosa and Mycoplana segnis. Int J Syst Evol Micr 40(4):434–442Google Scholar
  121. Urakawa H, Tajima Y, Numata Y, Tsuneda S (2008) Low temperature decreases the phylogenetic diversity of ammonia-oxidizing archaea and bacteria in aquarium biofiltration systems. Appl Environ Microb 74(3):894–900Google Scholar
  122. Vasanthakumar A, Handelsman J, Schloss PD, Bauer LS, Raffa KF (2008) Gut microbiota of an invasive subcortical beetle, Agrilus planipennis Fairmaire, across various life stages. Environ Entomol 37(5):1344–1353PubMedGoogle Scholar
  123. von Siebenthal BA, Jacob A, Wedekind C (2009) Tolerance of whitefish embryos to Pseudomonas fluorescens linked to genetic and maternal effects, and reduced by previous exposure. Fish Shellfish Immun 26:531–535Google Scholar
  124. von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21(3):213–229Google Scholar
  125. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73(16):5261–5267Google Scholar
  126. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3(1):89–101Google Scholar
  127. Watson SW, Bock E, Valois FW, Waterbury JB, Schlosser U (1986) Nitrospira marina gen. nov., sp. nov., a chemolithotrophic nitrite-oxidizing bacterium. Arch Microbiol 144(1):1–7Google Scholar
  128. Wedekind C (2002) Induced hatching to avoid infectious egg disease in whitefish. Curr Biol 12(1):69–71PubMedGoogle Scholar
  129. Wedekind C, Walker M, Portmann J, Cenni B, Müller R, Binz T (2004) MHC-linked susceptibility to a bacterial infection, but no MHC-linked cryptic female choice in whitefish. J Evol Biol 17(1):11–18PubMedGoogle Scholar
  130. Wedekind C, von Siebenthal B, Gingold R (2007) The weaker points of fish acute toxicity tests and how tests on embryos can solve some issues. Environ Pollut 148(2):385–389PubMedGoogle Scholar
  131. Wedekind C, Gessner MO, Vazquez F, Märki M, Steiner D (2010) Elevated resource availability sufficient to turn opportunistic into virulent fish pathogens. Ecology 91(5):1251–1256PubMedGoogle Scholar
  132. Willems A, Busse J, Goor M, Pot B, Falsen E, Jantzen E, Hoste B, Gillis M, Kersters K, Auling G, Deley J (1989) Hydrogenophaga, a new genus of hydrogen-oxidizing bacteria that includes Hydrogenophaga flava comb. nov. (formerly Pseudomonas flava), Hydrogenophaga palleronii (formerly Pseudomonas palleronii), Hydrogenophaga pseudoflava (formerly Pseudomonas pseudoflava and Pseudomonas carboxydoflava), and Hydrogenophaga taeniospiralis (formerly Pseudomonas taeniospiralis). Int J Syst Bacteriol 39(3):319–333Google Scholar
  133. Wisz MS, Pottier J, Kissling WD, Pellissier L, Lenoir J, Damgaard CF, Dormann CF, Forchhammer MC, Grytnes JA, Guisan A, Heikkinen RK, Hoye TT, Kuhn I, Luoto M, Maiorano L, Nilsson MC, Normand S, Ockinger E, Schmidt NM, Termansen M, Timmermann A, Wardle DA, Aastrup P, Svenning JC (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol Rev 88(1):15–30PubMedCentralPubMedGoogle Scholar
  134. Wu ML, van Teeseling MCF, Willems MJR, van Donselaar EG, Klingl A, Rachel R, Geerts WJC, Jetten MSM, Strous M, van Niftrik L (2012) Ultrastructure of the denitrifying methanotroph “Candidatus Methylomirabilis oxyfera,” a novel polygon-shaped bacterium. J Bacteriol 194(2):284–291PubMedCentralPubMedGoogle Scholar
  135. Xu JP (2006) Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Mol Ecol 15(7):1713–1731PubMedGoogle Scholar
  136. Ye L, Amberg J, Chapman D, Gaikowski M, Liu WT (2013) Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J 8(10):541–551PubMedCentralPubMedGoogle Scholar
  137. Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Micr 53:1155–1163Google Scholar
  138. Zogg GP, Zak DR, Ringelberg DB, MacDonald NW, Pregitzer KS, White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61(2):475–481Google Scholar

Copyright information

© Springer Basel 2015

Authors and Affiliations

  • Laetitia G. E. Wilkins
    • 1
  • Aude Rogivue
    • 1
    • 2
  • Luca Fumagalli
    • 1
  • Claus Wedekind
    • 1
  1. 1.Department of Ecology and Evolution, BiophoreUniversity of LausanneLausanneSwitzerland
  2. 2.WSL Swiss Federal Research InstituteBirmensdorfSwitzerland

Personalised recommendations