Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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):1–7

    CAS  PubMed  Google Scholar 

  • Amann R, Ludwig W (2000) Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol Rev 24(5):555–565

    CAS  PubMed  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26(1):32–46

    Google Scholar 

  • Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1):245–253

    PubMed  Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84(2):511–525

    Google Scholar 

  • 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):33–39

    CAS  PubMed  Google Scholar 

  • Austin B, Austin DA (2007) Bacterial fish pathogens: diseases of farmed and wild fish, 5th edn. Springer, London

    Google Scholar 

  • 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):691–703

    CAS  PubMed  Google Scholar 

  • Behar A, Yuval B, Jurkevitch E (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol 14(9):2637–2643

    CAS  PubMed  Google Scholar 

  • Berry D, Ben Mahfoudh K, Wagner M, Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microb 77(21):7846–7849

    CAS  Google Scholar 

  • 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):1027–1039

    CAS  PubMed  Google Scholar 

  • 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):85–93

    CAS  PubMed  Google Scholar 

  • Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341(6146):667–669

    CAS  PubMed  Google Scholar 

  • 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):14288–14293

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):266–267

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):335–336

    CAS  PubMed Central  PubMed  Google Scholar 

  • Casadevall A, Pirofski LA (1999) Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 67(8):3703–3713

    CAS  PubMed Central  PubMed  Google Scholar 

  • Casadevall A, Pirofski LA (2000) Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun 68(12):6511–6518

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 10:2–6

    Google Scholar 

  • 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):5256–5269

    CAS  PubMed  Google Scholar 

  • 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 28:714–723

    Google Scholar 

  • 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–D296

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):1228–1231

    CAS  PubMed  Google Scholar 

  • 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):1694–1697

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):177–186

    CAS  PubMed  Google Scholar 

  • 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):e46662

    CAS  PubMed Central  PubMed  Google Scholar 

  • Denton M, Kerr KG (1998) Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 11(1):57–80

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92

    CAS  PubMed  Google Scholar 

  • Douglas AE (1994) Symbiotic interactions. Oxford University Press, Oxford

    Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    CAS  PubMed  Google Scholar 

  • 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):16–23

    CAS  PubMed  Google Scholar 

  • 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):116–121

    Google Scholar 

  • Ellis AE (2001) Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol 25(8–9):827–839

    CAS  PubMed  Google Scholar 

  • 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):4716–4729

    CAS  PubMed  Google Scholar 

  • Evans ML, Neff BD, Heath DD (2010) MHC-mediated local adaptation in reciprocally translocated Chinook salmon. Conserv Genet 11(6):2333–2342

    CAS  Google Scholar 

  • 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):4038–4050

    CAS  PubMed  Google Scholar 

  • 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):6477–6481

    CAS  PubMed Central  PubMed  Google Scholar 

  • Finn RN (2007) The physiology and toxicology of salmonid eggs and larvae in relation to water quality criteria. Aquat Toxicol 81(4):337–354

    CAS  PubMed  Google Scholar 

  • 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):3784–3792

    Google Scholar 

  • Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11(8):e1001631

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):1197–1206

    CAS  Google Scholar 

  • 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):e15545

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):991–1006

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 195–211

  • 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 60:166–173

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):235–237

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):411–435

    CAS  Google Scholar 

  • 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):10–26

    Google Scholar 

  • 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):1113–1127

    CAS  Google Scholar 

  • 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):62–69

    CAS  PubMed  Google Scholar 

  • Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43(1):1–11

    CAS  PubMed  Google Scholar 

  • Hollander M, Wolfe DA (1973) Nonparametric statistical methods, 2nd edn. Wiley, New York

    Google Scholar 

  • Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292(5519):1115–1118

    CAS  PubMed  Google Scholar 

  • Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307

    CAS  PubMed  Google Scholar 

  • Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2002) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microb 68(1):448

    CAS  Google Scholar 

  • 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):e1000255

    PubMed Central  PubMed  Google Scholar 

  • Hutchings JA, Morris DW (1985) The influence of phylogeny, size and behavior on patterns of covariation in salmonid life histories. Oikos 45(1):118–124

    Google Scholar 

  • 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 54:1773–1788

    CAS  PubMed  Google Scholar 

  • 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):5296–5307

    PubMed  Google Scholar 

  • Johnson DR, Goldschmidt F, Lilja EE, Ackermann M (2012) Metabolic specialization and the assembly of microbial communities. ISME J 6(11):1985–1991

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):7210–7215

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jung A, Jung-Schroers V (2011) Detection of Deefgea chitinilytica in freshwater ornamental fish. Lett Appl Microbiol 52(5):497–500

    CAS  PubMed  Google Scholar 

  • 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):5231–5236

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim S, Gong G, Park TH, Um Y (2013) Asticcacaulis solisilvae sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 63:3829–3834

    CAS  PubMed  Google Scholar 

  • Kojima H, Fukui M (2011) Sulfuritalea hydrogenivorans gen. nov., sp. nov., a facultative autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 61:1651–1655

    CAS  PubMed  Google Scholar 

  • Kottelat M, Freyhof J (2007) Handbook of European Freshwater Fishes. Kottelat/Freyhof, Cornol/Berlin

    Google Scholar 

  • 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):e3249

    Google Scholar 

  • 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):483–494

    CAS  PubMed  Google Scholar 

  • 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):5111–5120

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 55:1907–1919

    CAS  PubMed  Google Scholar 

  • 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 62:259

    CAS  Google Scholar 

  • Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69(1):1–24

    Google Scholar 

  • 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):592–613

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):1647–1651

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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)

  • 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):168–179

    PubMed  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microb 71(12):8228–8235

    CAS  Google Scholar 

  • Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104(27):11436–11440

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5(2):169–172

    PubMed Central  PubMed  Google Scholar 

  • Luczynski M, Kirklewska A (1984) Dependence of Coregonus albula embryogenesis rate on the incubation temperature. Aquaculture 42(1):43–55

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Madigan MT, Martinko JM, Stahl D, Clark DP (2010) Brock biology of microorganisms, 13th edn. Benjamin Cummings, San Francisco

    Google Scholar 

  • 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):79–84

    CAS  Google Scholar 

  • 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):200–216

    Google Scholar 

  • 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):2960–2970

    CAS  PubMed  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82(1):290–297

    Google Scholar 

  • 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):610–618

    CAS  PubMed Central  PubMed  Google Scholar 

  • McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 105:87–116

    Google Scholar 

  • 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):568–580

    CAS  PubMed  Google Scholar 

  • Müller R, Stadelmann P (2004) Fish habitat requirements as the basis for rehabilitation of eutrophic lakes by oxygenation. Fish Manag Ecol 11(3–4):251–260

    Google Scholar 

  • Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267

    CAS  PubMed  Google Scholar 

  • 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 2:200–208

    PubMed Central  PubMed  Google Scholar 

  • 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 2.0-8

  • 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):e60811

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):1112–1115

    PubMed Central  PubMed  Google Scholar 

  • 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):435–439

    CAS  Google Scholar 

  • 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):3833–3849

    CAS  PubMed  Google Scholar 

  • 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):2357–2365

    CAS  PubMed  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2008) FastBLAST: homology relationships for millions of proteins. PLoS One 3(10):e3589

    PubMed Central  PubMed  Google Scholar 

  • Qi WH, Nong G, Preston JF, Ben-Ami F, Ebert D (2009) Comparative metagenomics of Daphnia symbionts. BMC Genomics 10(1):172

  • 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 108:4680–4687

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):e1002815

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):689–692

    CAS  PubMed  Google Scholar 

  • 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):422–430

    CAS  PubMed  Google Scholar 

  • 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):355–362

    CAS  PubMed  Google Scholar 

  • 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):224–233

    CAS  PubMed  Google Scholar 

  • 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):127–134

    CAS  Google Scholar 

  • 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):5900–5907

    CAS  Google Scholar 

  • Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6(8):229

    PubMed Central  PubMed  Google Scholar 

  • 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):e27310

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):383–393

    PubMed Central  PubMed  Google Scholar 

  • 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):1029–1046

    CAS  PubMed  Google Scholar 

  • 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):2153–2167

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):199–219

    CAS  Google Scholar 

  • Shin YK, Hiraishi A, Sugiyama J (1993) Molecular systematics of the genus Zoogloea and emendation of the genus. Int J Syst Bacteriol 43(4):826–831

    CAS  PubMed  Google Scholar 

  • 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):631–639

    CAS  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Treasurer JW, Cochrane E, Grant A (2005) Surface disinfection of cod Gadus morhua and haddock Melanogrammus aeglefinus eggs with bronopol. Aquaculture 250(1–2):27–35

    CAS  Google Scholar 

  • 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):434–442

    CAS  Google Scholar 

  • 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):894–900

    CAS  Google Scholar 

  • 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):1344–1353

    PubMed  Google Scholar 

  • 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 26:531–535

    Google Scholar 

  • 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):213–229

    Google Scholar 

  • 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):5261–5267

    CAS  Google Scholar 

  • Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3(1):89–101

    Google Scholar 

  • 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):1–7

    Google Scholar 

  • Wedekind C (2002) Induced hatching to avoid infectious egg disease in whitefish. Curr Biol 12(1):69–71

    CAS  PubMed  Google Scholar 

  • 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):11–18

    CAS  PubMed  Google Scholar 

  • 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):385–389

    CAS  PubMed  Google Scholar 

  • 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):1251–1256

    CAS  PubMed  Google Scholar 

  • 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):319–333

    CAS  Google Scholar 

  • 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):15–30

    PubMed Central  PubMed  Google Scholar 

  • 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):284–291

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu JP (2006) Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Mol Ecol 15(7):1713–1731

    CAS  PubMed  Google Scholar 

  • 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):541–551

    PubMed Central  PubMed  Google Scholar 

  • 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 53:1155–1163

    CAS  Google Scholar 

  • 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):475–481

    CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolution, Biophore, University of Lausanne, 1015, Lausanne, Switzerland

    Laetitia G. E. Wilkins, Aude Rogivue, Luca Fumagalli & Claus Wedekind

  2. WSL Swiss Federal Research Institute, Zürcherstrasse 111, 8903, Birmensdorf, Switzerland

    Aude Rogivue

Authors
  1. Laetitia G. E. Wilkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aude Rogivue
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luca Fumagalli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claus Wedekind
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laetitia G. E. Wilkins.

Additional information

L. Fumagalli and C. Wedekind are joint senior authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 954 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wilkins, L.G.E., Rogivue, A., Fumagalli, L. et al. Declining diversity of egg-associated bacteria during development of naturally spawned whitefish embryos (Coregonus spp.). Aquat Sci 77, 481–497 (2015). https://doi.org/10.1007/s00027-015-0392-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-015-0392-9

Keywords

Search

Navigation