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The emergence of epitheliocystis in the upper Rhone region: evidence for Chlamydiae in wild and farmed salmonid populations

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Abstract

We present the first study comparing epitheliocystis in a wild and farmed salmonid in Europe. Sampling three tributaries to the Lake Geneva, including one from headwaters to river mouth, revealed an unequal distribution of epitheliocystis in brown trout (Salmo trutta). When evaluated histologically and comparing sites grouped as wild versus farm, the probability of finding infected trout is higher on farms. In contrast, the infection intensities, as estimated by the number of cysts per gill arch, were higher on average and showed maximum values in the wild trout. Sequence analysis showed the most common epitheliocystis agents were Candidatus Piscichlamydia salmonis, all clustering into a single clade, whereas Candidatus Clavichlamydia salmonicola sequences cluster in two closely related subspecies, of which one was mostly found in farmed fish and the other exclusively in wild brown trout, indicating that farms are unlikely to be the source of infections in wild trout. A detailed morphological analysis of cysts using transmission electron microscopy revealed unique features illustrating the wide divergence existing between Ca. P. salmonis and Ca. C. salmonicola within the phylum Chlamydiae.

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References

  • Abowei JFN, Briyani OF (2011) A review of some bacterial diseases in African culture fisheries. Asian J Med Sci 3(5):206–217

    Google Scholar 

  • Contador E, Methner P, Ryerse I, Huber P, Lillie BN, Frasca S Jr, Lumsden JS (2015) Epitheliocystis in lake trout Salvelinus namaycush (Walbaum) is associated with a beta-proteobacteria. J Fish Dis. doi:10.1111/jfd.12369

    PubMed  Google Scholar 

  • Crespo S, Zarza C, Padros F, Marin de Mateo M (1999) Epitheliocystis agents in sea bream Sparus aurata: morphological evidence for two distinct chlamydia-like developmental cycles. Dis Aquat Org 37:61–72

    Article  CAS  PubMed  Google Scholar 

  • Crespo S, Zarza C, Padros F (2001) Epitheliocystis hyperinfection in sea bass, Dicentrarchus labrax (L.): light and electron microscope observations. J Fish Dis 24:557–560

    Article  Google Scholar 

  • Draghi A, Popov VL, Kahl MM, Stanton JB, Brown CC, Tsongalis GJ, West AB, Frasca S Jr (2004) Characterization of “Candidatus Piscichlamydia salmonis” (Order Chlamydiales), a Chlamydia-like bacterium associated with epitheliocystis in farmed Atlantic salmon (Salmo salar). J Clin Microbiol 42:5286–5297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Draghi A, Bebak J, Popov VL, Noble AC, Geary SJ, West AB, Philip B, Salvatore F (2007) Characterization of a Neochlamydia-like bacterium associated with epitheliocystis in cultured Arctic charr Salvelinus alpinus. Dis Aquat Org 76:27–38

    Article  CAS  PubMed  Google Scholar 

  • Draghi A, Bebak J, Daniel S, Tulman ER, Geary SJ, West AB, Popov VL, Frasca S Jr (2010) Identification of ‘Candidatus Piscichlamydia salmonis’ in Arctic charr Salvelinus alpinus during a survey of charr production facilities in North America. Dis Aquat Org 89:39–49

    Article  CAS  PubMed  Google Scholar 

  • Everett KDE, Hornung LJ, Andersen AA (1999) Rapid detection of the Chlamydiaceae and other families in the order Chlamydiales: three PCR tests. J Clin Microbiol 37:575–580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fehr A, Walther E, Schmidt-Posthaus H, Nufer L, Wilson A, Svercel M, Richter D, Segner H, Pospischil A, Vaughan L (2013) Candidatus Syngnamydia venezia, a novel member of the phylum Chlamydiae from the broad nosed pipefish, Syngnathus typhle. PLoS One 8:e70853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224

    Article  CAS  PubMed  Google Scholar 

  • Hoffman GL, Dunbar CE, Wolf K, Zwillenberg LO (1969) Epitheliocystis, a new infectious disease of the bluegill (Lepomis macrochirus). A van Leeuw 35:146–158

    Article  CAS  Google Scholar 

  • Karlsen M, Nylund A, Watanabe K, Helvik JV, Nylund S, Plarre H (2008) Characterization of ‘Candidatus Clavochlamydia salmonicola’: an intracellular bacterium infecting salmonid fish. Environ Microbiol 10:208–218

    CAS  PubMed  Google Scholar 

  • Lewis EJ, McLaughlin SM, Bodammer JE, Sawyer TK (1992) Epitheliocystis in ten new host species of marine fish. J Fish Dis 15:267–271

    Article  Google Scholar 

  • Mitchell SO, Steinum T, Rodger H, Holland C, Falk K, Colquhoun DJ (2010) Epitheliocystis in Atlantic salmon, Salmo salar L., farmed in fresh water in Ireland is associated with ‘Candidatus Clavochlamydia salmonicola’ infection. J Fish Dis 33(8):665–673

    Article  CAS  PubMed  Google Scholar 

  • Mitchell SO, Steinum T, Toenshoff ER, Kvellestad A, Falk K, Horn M, Colquhoun DJ (2013) ‘Candidatus Branchiomonas cysticola’ is a common agent of epitheliocysts in seawater-farmed Atlantic salmon Salmo salar in Norway and Ireland. Dis Aquat Org 103:35–43

    Article  CAS  PubMed  Google Scholar 

  • Nowak BF, LaPatra SE (2006) Epitheliocystis in fish. J Fish Dis 29:573–588

    Article  CAS  PubMed  Google Scholar 

  • Nylund A, Kvenseth AM, Isdal E (1998) A morphological study of the epitheliocystis agent in farmed Atlantic salmon. J Aquat Anim Health 10:43–55

    Article  Google Scholar 

  • Paperna I (1977) Epitheliocystis infection in wild and cultured sea bream (Sparus auratus, Sparidae) and grey mullets (Liza ramada, Mugilidae). Aquaculture 10:169–176

    Article  Google Scholar 

  • Paperna I, Sabnai I (1980) Epitheliocystis disease in fish. In: Ahne W (ed) Fish diseases, Third COPRAQ-Session. Springer, Berlin, pp 228–234

    Chapter  Google Scholar 

  • Schmidt-Posthaus H, Bernet D, Wahli T, Burkhardt-Holm P (2001) Morphological organ alterations and infectious diseases in brown trout (Salmo trutta) and rainbow trout (Onchorhynchus mykiss) exposed to polluted river water. Dis Aquat Org 44:161–170

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Posthaus H, Polkinghorne A, Nufer L, Schifferli A, Zimmermann DR, Segner H, Steiner P, Vaughan L (2012) A natural freshwater origin for two chlamydial species, Candidatus Piscichlamydia salmonis and Candidatus Clavochlamydia salmonicola, causing mixed infections in wild brown trout (Salmo trutta). Environ Microbiol 14:2048–2057

    Article  PubMed  Google Scholar 

  • Segner H, Sundh H, Buchmann K, Douxfils J, Sundell KS, Mathieu C, Ruane N, Jutfelt F, Toften H, Vaughan L (2011) Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiol Biochem 38:85–105

    Article  PubMed  Google Scholar 

  • Steigen A, Nylund A, Karlsbakk E, Akoll P, Fiksdal IU, Nyland S, Odong R, Plarre H, Semyalo R, Skår C, Watanabe K (2013) ‘Cand. Actinochlamydia clariae’ gen. nov., sp. nov., a unique intracellular bacterium causing epitheliocystis in catfish (Clarias gariepinus) in Uganda. PLoS One 8:e66840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steigen A, Karlsbakk E, Plarre H, Watanabe K, Øvergård AC, Brevik Ø, Nylund A (2015) A new intracellular bacterium, Candidatus Similichlamydia labri sp. nov. (Chlamydiaceae) producing epitheliocysts in ballan wrasse, Labrus bergylta (Pisces, Labridae). Arch Microbiol 197:311–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stride MC, Polkinghorne A, Miller TL, Groff JM, LaPatra SE, Nowak BF (2013a) Molecular characterization of “Candidatus Parilichlamydia carangidicola”, a novel Chlamydia-like epitheliocystis agent in yellowtail kingfish, Seriola lalandi (Valenciennes), and the proposal of a new family, “Candidatus Parilichlamydiaceae” fam. nov. (order Chlamydiales). Appl Environ Microbiol 79:1590–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stride MC, Polkinghorne A, Miller TL, Nowak BF (2013b) Molecular characterization of “Candidatus Similichlamydia latridicola” gen. nov., sp. nov. (Chlamydiales: “Candidatus Parilichlamydiaceae”), a novel Chlamydia-like epitheliocystis agent in the striped trumpeter, Latris lineata (Forster). Appl Environ Microbiol 79:4914–4920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stride MC, Polkinghorne A, Nowak BF (2014) Chlamydial infections of fish: diverse pathogens and emerging causes of disease in aquaculture species. Vet Microbiol 170:19–27

    Article  CAS  PubMed  Google Scholar 

  • Toenshoff ER, Kvellestad A, Mitchell SO, Steinum T, Falk K, Colquhoun DJ, Horn M (2012) A novel betaproteobacterial agent of gill epitheliocystis in seawater farmed Atlantic salmon (Salmo salar). PLoS One 7:e32696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank the fish farmers at the Venoge who provided the brown trout for examination. Further we thank Aurelie Rubin and the team of the Centre for Fish and Wildlife Health, Bern for help during the sampling. This study was partly financed by the ESKAS-Bundesstipendien für ausländische Studierende, Kunstschaffende und Forschende, Bern, Switzerland.

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Authors and Affiliations

  1. Centre of Fish and Wildlife Health, Department of Infectious Diseases and Pathobiology, University of Bern, Bern, Switzerland

    Maricruz Guevara Soto, Helmut Segner & Heike Schmidt-Posthaus

  2. Institute of Veterinary Public Health, University of Bern, Bern, Switzerland

    Beatriz Vidondo

  3. Institute of Veterinary Pathology, University of Zurich, Zurich, Switzerland

    Lloyd Vaughan & Lisbeth Nufer

  4. Functional Genomics Center Zurich, University of Zurich, Zurich, Switzerland

    Helena M. B. Seth-Smith

  5. Fondation de la Maison de la Rivière, Tolochenaz, Switzerland

    Jean-Francois Rubin

Authors
  1. Maricruz Guevara Soto
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  2. Beatriz Vidondo
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  3. Lloyd Vaughan
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  4. Helena M. B. Seth-Smith
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  5. Lisbeth Nufer
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  6. Helmut Segner
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  7. Jean-Francois Rubin
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  8. Heike Schmidt-Posthaus
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Correspondence to Heike Schmidt-Posthaus.

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The authors declare they have no competing interests and they were notified about the content of the manuscript.

Animal rights statement

All animals were treated according to the Swiss welfare regulations (permission number: 2871).

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Communicated by Erko Stackebrandt.

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Guevara Soto, M., Vidondo, B., Vaughan, L. et al. The emergence of epitheliocystis in the upper Rhone region: evidence for Chlamydiae in wild and farmed salmonid populations. Arch Microbiol 198, 315–324 (2016). https://doi.org/10.1007/s00203-016-1192-x

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  • DOI: https://doi.org/10.1007/s00203-016-1192-x

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