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Cryptic Infection of a Broad Taxonomic and Geographic Diversity of Tadpoles by Perkinsea Protists

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Cryptic Infection of a Broad Taxonomic and Geographic Diversity of Tadpoles by Perkinsea Protists Cryptic infection of a broad taxonomic and geographic PNAS PLUS diversity of tadpoles by Perkinsea protists Aurélie Chambouveta,b,1, David J. Gowerb, Miloslav Jirkuc, Michael J. Yabsleyd,e, Andrew K. Davisf, Guy Leonarda, Finlay Maguireb,g, Thomas M. Doherty-Boneb,h,i, Gabriela Bueno Bittencourt-Silvaj, Mark Wilkinsonb, and Thomas A. Richardsa,k,1 aBiosciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4QD, United Kingdom; bDepartment of Life Sciences, The Natural History Museum, London SW7 5BD, United Kingdom; cInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 Ceske Budejovice, Czech Republic; dWarnell School of Forestry and Natural Resources, The University of Georgia, Athens, GA 30602; eSoutheastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, The University of Georgia, Athens, GA 30602; fOdum School of Ecology, The University of Georgia, Athens, GA 30602; gGenetics, Ecology and Evolution, University College London, London WC1E 6BT, United Kingdom; hSchool of Geography, University of Leeds, Leeds LS2 9JT, United Kingdom; iSchool of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom; jDepartment of Environmental Sciences, University of Basel, CH-4056 Basel, Switzerland; and kCIFAR Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced Research, Toronto, ON, Canada M5G 1Z8 Edited by Francisco J. Ayala, University of California, Irvine, CA, and approved July 6, 2015 (received for review January 5, 2015) The decline of amphibian populations, particularly frogs, is often spherical cells preferentially infecting livers of tadpoles of the cited as an example in support of the claim that Earth is un- Southern Leopard Frog (Lithobates sphenocephalus, formerly dergoing its sixth mass extinction event. Amphibians seem to be Rana sphenocephala) sampled from an MME in Georgia (United particularly sensitive to emerging diseases (e.g., fungal and viral States) (12). Small subunit (SSU) ribosomal DNA (rDNA) PCR pathogens), yet the diversity and geographic distribution of in- and direct-amplicon sequencing, combined with phylogenetic fectious agents are only starting to be investigated. Recent work tree reconstruction, showed that a lineage of protists closely has linked a previously undescribed protist with mass-mortality related to Perkinsus, a parasite of marine bivalves (14), was the events in the United States, in which infected frog tadpoles have likely infectious agent (12). an abnormally enlarged yellowish liver filled with protist cells of a Perkinsea alveolates were first described as being affiliated presumed parasite. Phylogenetic analyses revealed that this in- with the Apicomplexa (14, 15), which includes important human fectious agent was affiliated with the Perkinsea: a parasitic group pathogens such as Toxoplasma gondii and Plasmodium spp. (the within the alveolates exemplified by Perkinsus sp., a “marine” pro- causative agents of malaria). Phylogenetic analysis has shown tist responsible for mass-mortality events in commercial shellfish that Perkinsea are a deeply divergent sister-group of dinoflagellate populations. Using small subunit (SSU) ribosomal DNA (rDNA) se- alveolates (16). Only three representative groups of Perkinsea quencing, we developed a targeted PCR protocol for preferentially were previously described morphologically and taxonomically: sampling a clade of the Perkinsea. We tested this protocol on Perkinsus spp., parasites of marine bivalves (e.g., oysters and freshwater environmental DNA, revealing a wide diversity of Per- clams), Parvilucifera spp., parasites of dinoflagellates, and Ras- kinsea lineages in these environments. Then, we used the same trimonas subtilis (previously Cryptophagus subtilis), parasites of protocol to test for Perkinsea-like lineages in livers of 182 tadpoles cryptophyte algae (17–20). However, environmental sequence from multiple families of frogs. We identified a distinct Perkinsea clade, encompassing a low level of SSU rDNA variation different from the lineage previously associated with tadpole mass-mortal- Significance ity events. Members of this clade were present in 38 tadpoles sampled from 14 distinct genera/phylogroups, from five countries Amphibians are among the most threatened animal groups. across three continents. These data provide, to our knowledge, the Population declines and extinctions have been linked, in part, first evidence that Perkinsea-like protists infect tadpoles across a to emerging infectious diseases. One such emerging disease wide taxonomic range of frogs in tropical and temperate environ- has been attributed to Perkinsea-like protists causing mass ments, including oceanic islands. mortality events in the United States. Using molecular meth- ods, we evaluated the diversity of Perkinsea parasites in livers frog decline | emerging disease | parasite | alveolates | molecular diversity sampled from a wide taxonomic collection of tadpoles from six countries across three continents. We discovered a previously unidentified phylogenetically distinct infectious agent of tad- t is widely recognized that amphibians are among the most ECOLOGY pole livers present in a broad range of frogs from both tropical threatened animal groups: for example, in 2008, 32% of species I and temperate sites and across all sampled continents. These were listed as “threatened or extinct” and 42% were listed as in data demonstrate the high prevalence and global distribution decline (www.iucnredlist.org/initiatives/amphibians/analysis; accessed of this infectious protist. October 29, 2014) (1, 2). The main causes of amphibian decline have been identified as habitat loss, environmental change, and Author contributions: A.C. and T.A.R. designed research; A.C. and D.J.G. performed re- the introduction of nonnative species (e.g., refs. 3–6). Emerging search; D.J.G., M.J., A.K.D., and G.B.B.-S. contributed new reagents/analytic tools; A.C., infectious diseases have also been shown to play a key role in G.L., F.M., T.M.D.-B., and T.A.R. analyzed data; A.C., D.J.G., M.J.Y., M.W., and T.A.R. wrote the paper; and D.J.G., M.J., M.J.Y., A.K.D., T.M.D.-B., G.B.B.-S., and M.W. collected many amphibian declines: for example, the chytrid fungal path- field samples. ogen Batrachochytrium dendrobatidis has caused mass mortality The authors declare no conflict of interest. events (MMEs) in Australia, in Europe, and across the Americas This article is a PNAS Direct Submission. (e.g., refs. 7–9). MMEs have also been associated with infection by Ranavirus in, for example, the United Kingdom (UK), United Freely available online through the PNAS open access option. Data deposition: The sequences reported in this paper have been deposited in the Gen- States (US), and Canada (10, 11). Recent work has linked local Bank database. For a list of accession numbers, see SI Appendix. MMEs in the United States with the infection of larval frogs 1To whom correspondence may be addressed. Email: [email protected] or (tadpoles) of the genera Lithobates and Acris by a protist (SI [email protected]. Appendix, Fig. S1) (12, 13). In 2006, histological examinations This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of tadpole tissues revealed the presence of thousands of small 1073/pnas.1500163112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1500163112 PNAS | Published online August 10, 2015 | E4743–E4751 Downloaded by guest on September 30, 2021 0.95/62/68 AB86FB Clade A Infectious 300FB 0.96/73/82 Clade B agent of tadpoles 5 Clade C V2 V3 V4 V7 1/99/100 1282R 1294R C 100 80 60 40 NAG01 Freshwater clone (AY919735) 20 % of clones assigned to clade A, B or C % of clones assigned to clade Freshwater clone (DQ244038) 0 Ranoidea Hyloidea Freshwater clone (EF196787) n1 = 148/31 n1 = 29/7 Clade A Clade B Clade C D n2=12/3 Freshwater clone (EU162626) n2=63/13 Freshwater clone (EU162629) n2=17/4 Infectious agent of tadpoles Davis et al. (EF675616) n2=16/4 n2=70/14 Clade A 1/94/80 Clade B Clade C Environmental sub-group 1 Marine clone (AF530536) Infectious PP/LogDet/ML UK samples: Freshwater clone (GQ330637) agent of ≥ 0.99/80/80 Perkinsus spp. bivalves Kennick reservoir Marine clone (FJ832127) Infectious agent ≥ 0.60/50/50 NHM pond (18/09/11) Parvilucifera spp. of dinoflagellates sequence from 2006 NHM pond (15/05/13) Environmental sub-group 2 mortality event Environmental sub-group 3 SL pond (15/05/13) s Environmental sub-group 4 French guiana samples: Tottiford reservoir Environmental sub-group 5 Environmental sub-group 6 T1 waterbody Trenchford reservoir Marine clone (AF530534) T2 waterbody Washington singer pond Marine clone (AJ402327) T6 waterbody Ullswater lake Outgroup 0.04 Fig. 1. (A) Phylogenetic tree of Perkinsea SSU rDNA sequences focusing on the NAG01 group that includes two separate phylogenetic groups recovered from tadpole liver tissue samples. The phylogeny is estimated from a masked alignment consisting of 292 taxa and 776 characters. Bayesian posterior probability (6,000 samples from 2,000,000 MCMCMC generations), LogDet distance bootstrap (1,000 pseudoreplicates), and maximum likelihood bootstrap (1,000 pseudoreplicates) values are added to each node using the following convention: support values are summarized by black circles when all are equal to or greater than 0.9/80%/80%, and white circles when the topology support is less but equal to or greater than 0.6/50%/50%. Five sequences of Amoebophrya
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