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Pathological and phylogenetic characterization of Amphibiothecum sp. infection in an isolated amphibian (Lissotriton helveticus) population on the island of Rum (Scotland)

Published online by Cambridge University Press:  22 November 2016

CATERINA FIEGNA ,
CHARLOTTE L. CLARKE ,
DARREN J. SHAW ,
JOHANNA L. BAILY ,
FRANCES C. CLARE ,
ALEXANDRA GRAY ,
TRENTON W. J. GARNER  and
ANNA L. MEREDITH
CATERINA FIEGNA
Affiliation:
Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Roslin EH25 9RG, UK
CHARLOTTE L. CLARKE*
Affiliation:
Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Roslin EH25 9RG, UK Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY London, UK
DARREN J. SHAW
Affiliation:
Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Roslin EH25 9RG, UK
JOHANNA L. BAILY
Affiliation:
Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Roslin EH25 9RG, UK
FRANCES C. CLARE
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY London, UK
ALEXANDRA GRAY
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY London, UK
TRENTON W. J. GARNER
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY London, UK
ANNA L. MEREDITH
Affiliation:
Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Roslin EH25 9RG, UK
*
*Corresponding author: Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Roslin, EH25 9RG, UK and Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY London, UK. E-mail: [email protected]
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Summary

Outbreaks of cutaneous infectious disease in amphibians are increasingly being attributed to an overlooked group of fungal-like pathogens, the Dermocystids. During the last 10 years on the Isle of Rum, Scotland, palmate newts (Lissotriton helveticus) have been reportedly afflicted by unusual skin lesions. Here we present pathological and molecular findings confirming that the pathogen associated with these lesions is a novel organism of the order Dermocystida, and represents the first formally reported, and potentially lethal, case of amphibian Dermocystid infection in the UK. Whilst the gross pathology and the parasite cyst morphology were synonymous to those described in a study from infected L. helveticus in France, we observed a more extreme clinical outcome on Rum involving severe subcutaneous oedema. Phylogenetic topologies supported synonymy between Dermocystid sequences from Rum and France and as well as their distinction from Amphibiocystidium spp. Phylogenetic analysis also suggested that the amphibian-infecting Dermocystids are not monophyletic. We conclude that the L. helveticus-infecting pathogen represents a single, novel species; Amphibiothecum meredithae.

Keywords

AmphibiocystidiumDermocystidiumAmphibiothecumpalmate newtsinfectionpathologyphylogenetics
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 484 - 496
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Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

†

Co-first authors.

References

REFERENCES

Anderson, L. (2010). Investigating the distribution and prevalence of a recently emerged parasite threatening palmate newts (Lissotriton helveticus) on the Isle of Rum. Master's Thesis (unpublished). Institute of Zoology, London.Google Scholar
Annis, S. L., Dastoor, F. P., Ziel, H., Daszak, P. and Longcore, J. E. (2004). A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. Journal of Wildlife Diseases 40, 420–428.Google Scholar
AVMA (2007). American Veterinary Medical Association Guidelines on Euthanasia (Formerly the Report of the AVMA Panel on Euthanasia), http://www.avma.org/issues/animal_welfare/euthanasia.pdf Google Scholar
Bandín, I. and Dopazo, C. (2011). Host range, host specificity and hypothesized host shift events among viruses of lower vertebrates. Veterinary Research 42, 1–16.CrossRefGoogle ScholarPubMed
Berger, L., Speare, R., Daszak, P., Green, D. E., Cunningham, A. A., Goggin, C. L., Slocombe, R., Ragan, M. A., Hyatt, A. D., McDonald, K. R., Hines, H. B., Lips, K. R., Marantelli, G. and Parkes, H. (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rainforests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95, 9031–9036.Google Scholar
Berger, L., Speare, R. and Hyatt, A. (1999). Chytrid fungi and amphibian declines: overview, implications and future directions. In Declines and Disappearances of Australian Frogs (ed. Campbell, A.), pp. 21–31. Environment Australia, Canberra, Australia.Google Scholar
Blaustein, A. R. and Wake, D. B. (1990). Declining amphibian populations – a global phenomenon. Trends in Ecology & Evolution 5, 203–204.Google Scholar
Blaustein, A. R. and Wake, D. B. (1995). The puzzle of declining amphibian populations. Scientific American 272, 52–57.Google Scholar
Blaustein, A. R., Gervasi, S. S., Johnson, P. T. J., Hoverman, J. T., Belden, L. K., Bradley, P. W. and Xie, G. Y. (2012). Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 1688–1707.Google Scholar
Broz, O. and Privora, M. (1952). Two skin parasites of Rana temporaria: Dermocystidium ranae Guyenot et Naville and Dermosporidium granulosum n. sp. Parasitology 42, 65–69.Google Scholar
Clare, F., Daniel, O., Garner, T. and Fisher, M. (2016). Assessing the ability of swab data to determine the true burden of infection for the amphibian pathogen Batrachochytrium dendrobatisdis . Ecohealth 13, 360–367.CrossRefGoogle Scholar
Courtois, E. A., Cornuau, J. H., Loyau, A. and Schmeller, D. S. (2013). Distribution of Amphibiocystidium sp. in palmate newts (Lissotriton helveticus) in Ariege, France. Herpetology Notes 6, 539–543.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife threats to biodiversity and human health. Science 287, 443–449.Google Scholar
Densmore, C. L. and Green, D. E. (2007). Disease of amphibians. Institute for Laboratory Animal Research Journal 48, 235–254.Google Scholar
Duffus, A. L. J. and Cunningham, A. A. (2010). Major disease threats to European amphibians. Herpetological Journal 20, 117–127.Google Scholar
Feldman, S. H., Wimsatt, J. H. and Green, D. E. (2005). Phylogenetic classification of the frog pathogen Amphibiothecum (Dermosporidium) penneri based on small ribosomal subunit sequencing. Journal of Wildlife Disease 41, 701–706.CrossRefGoogle ScholarPubMed
Goodman, R. M., Miller, D. L. and Ararso, Y. T. (2013). Prevalence of Ranavirus in Virginia turtles as detected by tail-clip sampling versus oral-cloacal swabbing. Northeastern Naturalist 20, 325–332.Google Scholar
González-Hernández, M., Denoël, M., Duffus, A. J. L., Garner, T. W. J., Cunningham, A. A. and Acevedo-Whitehouse, K. (2010). Dermocystid infection and associated skin lesions in free-living palmate newts (Lissotriton helveticus) from Southern France. Parasitology International 59, 44–350.CrossRefGoogle ScholarPubMed
Granata, L. (1919). Dermocycoides beccarii n. g. n. sp. nuovo enigmatico parassita di Molge vulgaris. Monitore zoologico italiano, 20, 153–160.Google Scholar
Greer, A. L. and Collins, J. P. (2007). Sensitivity of a diagnostic test for amphibian Ranavirus varies with sampling protocol. Journal of Wildlife Diseases 43, 525–532.Google Scholar
Gray, A. (2008). Infection of the palmate newt (Triturus helveticus) by a novel species of Amphibiocystidium on the Isle of Rum, Scotland. Unpublished Master's Thesis. Institute of Zoology, London.Google Scholar
Gray, M. J., Miller, D. L. and Hoverman, J. T. (2012). Reliability of non-lethal surveillance methods for detecting Ranavirus infection. Diseases of Aquatic Organisms 99, 1–6.Google Scholar
Griffiths, R. A. (1996). Newts and Salamanders of Europe. T. & A.D. Poyser, London, 188 p.Google Scholar
Guyenot, E. and Naville, A. (1922). Un nouveau protiste du genre Dermocystidium parasite de la Grenouille Dermocystidium ranae nov. spec. Revue Suisse de Zoologie 29, 133–145.Google Scholar
Halliday, T. R. (1990). The evolution of courtship behavior in newts and salamanders. In Advances in the Study of Behavior 19 (ed. Peter, J. B., Slater, J. S. R. and Colin, B.), pp. 137–169. Academic Press, San Diego.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Herr, R. A., Ajello, L., Taylor, J. W., Arseculeratne, S. N. and Mendoza, L. (1999). Phylogenetic analysis of Rhinosporidium seeberi's 18S small-subunit ribosomal DNA groups this pathogen among members of the protoctistant mysomycetozoan clade. Journal of Clinical Microbiology 3, 2750–2754.CrossRefGoogle Scholar
Hasegawa, M., Kishino, H. and Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 21, 160–174.Google Scholar
Hosmer, D. W. and Lemeshow, S. (2000). Applied Logistic Regression. John Wiley and Sons, New York, USA.Google Scholar
Houlahan, J. E., Findlay, S. C., Schmidt, B. R., Meyer, A. H. and Kuzmin, S. L. (2000). Quantitative evidence for global amphibian population declines. Nature 404, 752–755.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P., Larget, B., and Alfaro, M. E. (2004). Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Molecular Biology and Evolution, 21, 1123–1133.CrossRefGoogle ScholarPubMed
Hyatt, A. D., Boyle, D. G., Olsen, V., Boyle, D. B., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F. and Colling, A. (2007). Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis . Diseases of Aquatic Organisms 73, 175–192.Google Scholar
Jancovich, J. K., Bremont, M., Touchman, J. W. and Jacobs, B. L. (2010). Evidence for multiple recent host species shifts among the Ranaviruses (Family Iridoviridae). Journal of Virology 84, 2636–2647.Google Scholar
Jay, J. M. and Pohley, W. J. (1981). Dermosporidium penneri sp n from the skin of the American toad, Bufo americanus (Amphibia, Bufonidae). Journal of Parasitology 67, 108–110.CrossRefGoogle Scholar
Larkin, M. A., Blackschiled, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Lips, K. R. (1999). Mass mortality and population declines of anurans at an upland site in Western Panama. Conservation Biology 13, 117–125.Google Scholar
Lips, K. R., Brem, F., Brenes, R., Reeve, J. D., Alford, R. A., Voyles, J., Carey, C., Livo, L., Pessier, A. P. and Collins, J. P. et al. (2006). Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America 103, 3165–3170.Google Scholar
Lindström, K. M., van der Veen, I. T., Legault, B-A. and Lundstroöm., J. O. (2003). Activity and predator escape performance of common Greenfinches Carduelis chloris infected with Sindbis virus. Ardea 91, 103–111.Google Scholar
Mendoza, L., Herr, R. A., Arseculerante, S. N. and Ajello, L. (1999). In vitro studies on the mechanisms of endospore release by Rhinosporidium seeberi . Mycopathologia 148, 9–15.Google Scholar
Mendoza, L., Taylor, J. W. and Ajello, L. (2002). The class Mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annual Reviews of Microbiology 56, 315–344.CrossRefGoogle ScholarPubMed
Olson, R. E., Dungan, C. F. and Holt, R. A. (1991). Water-borne transmission of Dermocystidium salmonis in the laboratory. Diseases of Aquatic Organisms 12, 41–48.CrossRefGoogle Scholar
Pascolini, R., Daszak, P., Cunningham, A. A., Tei, S., Vagnetti, D., Bucci, S., Fagotti, A. and Di Rosa, I. (2003). Parasitism by Dermocystidium ranae in a population of Ranaesculenta complex in Central Italy and description of Amphibiocystidium n. gen. Diseases of Aquatic Organisms 56, 65–74.Google Scholar
Pereira, C. N., Di Rosa, I., Fagotti, A., Simoncelli, F., Pascolini, R. and Mendoza, L. (2005). The pathogen of frogs Amphibiocystidium ranae is a member of the order Dermocystida in the class Mesomycetozoea. Journal of Clinical Microbiology 43, 192–198.Google Scholar
Perez, C. (1907). Dermocystidium pusula, organismenouveu parasite de lapeaudestritons. Comptesrendus de Seances de Societe de Biologie 63, 445–446.Google Scholar
Perez, C. (1913). Dermocystidium pusula: parasite de la peau des Tritons. Archives de Zoologie Experimentale et Generale 52, 343–357.Google Scholar
Perkins, F. O. (1976). Zoospores of the oyster pathogen Dermocystjdium marinum. I. Fine structure of the conoid and other sporozoan-like organelles. Journal of Parasitology 62, 959–974.Google Scholar
Poisson, C. (1937). Sur une nouvelle espèce du genre Dermomycoides Granata 1919: Dermomycoides armoriacus Poisson 1936 parasite cutane de Triturus palmatus (Schneider). Genèse et structure de la zoospore. Bulletin Biologique de la France et de la Belgique 71, 91–116.Google Scholar
Posada, D. and Crandall, K. A. (1998). ModelTest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Price, S. J., Garner, T. W. J., Nichols, R. A., Balloux, F., Ayres, C., Mora-Cabello de Alba, A. and Bosch, J. (2014). Collapse of amphibian communities due to an introduced Ranavirus. Current Biology 24, 2586–2591.Google Scholar
R Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Raffel, T. R., Bommarito, T., Barry, D. S., Witiak, S. M., and Shackelton, L. A. (2008). Widespread infection of the Eastern red-spotted newt (Notophthalmus viridescens) by a new species of Amphibiocystidium, a genus of fungus-like Mesomycetozoan parasites not previously reported in North America. Parasitology 135, 203–215.Google Scholar
Ragan, M. A., Goggin, C. L., Cawthorn, R. J., Cerenius, L., Jamieson, A. V. C., Plourde, S. M., Rand, T. G., Soderhall, K. and Gutell, R. R. (1996). A novel clade of protistan parasites near the animal-fungal divergence. Proceedings of National Academy of Sciences of the United States of America 93, 11907–11912.CrossRefGoogle ScholarPubMed
Rambaut, A. (2014). Figtree, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree Google Scholar
Ripplinger, J. and Sullivan, J. (2010). Assessment of substitution-model adequacy using frequentist and Bayesian methods. Molecular Biology and Evolution, 27, 2790–2803.Google Scholar
Roelants, K., Gower, D. J., Wilkinson, M., Loader, S. P., Biju, S. D., Guilaume, K., Moriau, L. and Bossuyt, F. (2007). Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences of the United States of America 104, 887–892.Google Scholar
Rollins-Smith, L. A. (2009). The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochimica et Biophysica Acta – Biomembranes 1788, 1593–1599.Google Scholar
Rollins-Smith, L. A., Doersam, J. K., Longcore, J. E., Taylor, S. K., Shamblin, J. C., Carey, C. and Zasloff, M. A. (2002). Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Developmental and Comparative Immunology 26, 63–72.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Rowley, J. J. L., Gleason, F. H., Andreou, D., Marshall, W., Lilje, O. and Goslan, R. (2013). Impacts of Mesomycetozoean parasites on amphibian and freshwater fish populations. Fungal Biology Reviews 27, 100–111.Google Scholar
Schwarz, G. E. (1978). Estimating the dimension of a model. Annals of Statistics, 6 (2), 461–464.Google Scholar
Shin, J., Bataille, A., Kosch, T. A. and Waldman, B. (2014). Swabbing often fails to detect amphibian Chytridiomycosis conditions of low infection load. PLoS ONE 9, e111091.CrossRefGoogle ScholarPubMed
Skerratt, L. F., Berger, L., Speare, R., Cashins, S., Mcdonald, K. R., Phillott, A., Hines, H. and Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.Google Scholar
Smith, K. G., Lips, K. R. and Chase, J. M. (2009). Selecting for extinction: nonrandom disease-associated extinction homogenizes amphibian biotas. Ecology Letters 12, 1069–1078.Google Scholar
Svennbland, B., Erixon, P., Oxelman, B. and Britton, T. (2006). Fundamental differences between the methods of maximum likelihood and maximum posterior probability in phylogenetics. Systematic Biology 55, 116–121.Google Scholar
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Thompson, J. D. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Vilela, R. and Mendoza, L. (2012). The taxonomy and phylogenetics of the human and animal pathogen Rhinosporidium seeberi: a critical review. Revista Iberoamericana de Micología 29, 185–199.Google Scholar
Woodhams, D. C., Rollins-Smith, L. A., Carey, C., Reinert, L. K., Tyler, M. J. and Alford, R. A. (2006). Population trends associated with skin peptide defenses against Chytridiomycosis in Australian frogs. Oecologia 146, 531–540.CrossRefGoogle ScholarPubMed
Woodhams, D. C., Rollins-Smith, L. A., Alford, R. A., Simon, M. A. and Harris, R. N. (2007). Innate immune defenses of amphibian skin: antimicrobial peptides and more. Animal Conservation 10, 425–428.Google Scholar
Yang, Z. and Rannala, B. (2012). Molecular phylogenetics: principles and practice. Nature Reviews Genetics 13, 303–314.Google Scholar
Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature 415, 389–395.Google Scholar
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