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Genomes of Fasciola Hepatica from the Americas Reveal Colonization with Neorickettsia Endobacteria Related to the Agents of Potomac Horse and Human Sennetsu Fevers

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Genomes of Fasciola Hepatica from the Americas Reveal Colonization with Neorickettsia Endobacteria Related to the Agents of Potomac Horse and Human Sennetsu Fevers RESEARCH ARTICLE Genomes of Fasciola hepatica from the Americas Reveal Colonization with Neorickettsia Endobacteria Related to the Agents of Potomac Horse and Human Sennetsu Fevers Samantha N. McNulty1, Jose F. Tort2, Gabriel Rinaldi3¤, Kerstin Fischer4, Bruce A. Rosa1, a1111111111 Pablo Smircich2, Santiago Fontenla2, Young-Jun Choi1, Rahul Tyagi1, a1111111111 Kymberlie Hallsworth-Pepin1, Victoria H. Mann3, Lakshmi Kammili5, Patricia S. Latham5, a1111111111 Nicolas Dell'Oca2, Fernanda Dominguez2, Carlos Carmona6, Peter U. Fischer4, Paul a1111111111 J. Brindley3, Makedonka Mitreva1,4* a1111111111 1 McDonnell Genome Institute at Washington University, St. Louis, Missouri, United States of America, 2 Departamento de GeneÂtica, Facultad de Medicina, Universidad de la RepuÂblica (UDELAR), Montevideo, Uruguay, 3 Department of Microbiology, Immunology and Tropical Medicine, and Research Center for Neglected Diseases of Poverty, School of Medicine & Health Sciences, George Washington University, Washington, DC, United States of America, 4 Division of Infectious Diseases, Department of Medicine, OPEN ACCESS Washington University School of Medicine, St. Louis, Missouri, United States of America, 5 Department of Pathology, School of Medicine & Health Sciences, George Washington University, Washington, DC, United Citation: McNulty SN, Tort JF, Rinaldi G, Fischer K, States of America, 6 Unidad de BiologõÂa Parasitaria, Instituto de BiologõÂa, Facultad de Ciencias, Instituto de Rosa BA, Smircich P, et al. (2017) Genomes of Higiene, Montevideo, Uruguay Fasciola hepatica from the Americas Reveal Colonization with Neorickettsia Endobacteria ¤ Current address: Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge, Related to the Agents of Potomac Horse and United Kingdom Human Sennetsu Fevers. PLoS Genet 13(1): * [email protected] e1006537. doi:10.1371/journal.pgen.1006537 Editor: Eva H. Stukenbrock, Max-Planck-Institut fur Evolutionsbiologie, GERMANY Abstract Received: June 9, 2016 Food borne trematodes (FBTs) are an assemblage of platyhelminth parasites transmitted Accepted: December 15, 2016 through the food chain, four of which are recognized as neglected tropical diseases (NTDs). Published: January 6, 2017 Fascioliasis stands out among the other NTDs due to its broad and significant impact on Copyright: © 2017 McNulty et al. This is an open both human and animal health, as Fasciola sp., are also considered major pathogens of access article distributed under the terms of the domesticated ruminants. Here we present a reference genome sequence of the common Creative Commons Attribution License, which liver fluke, Fasciola hepatica isolated from sheep, complementing previously reported iso- permits unrestricted use, distribution, and reproduction in any medium, provided the original late from cattle. A total of 14,642 genes were predicted from the 1.14 GB genome of the liver author and source are credited. fluke. Comparative genomics indicated that F. hepatica Oregon and related food-borne Data Availability Statement: All sequence data trematodes are metabolically less constrained than schistosomes and cestodes, taking from this project is available at NCBI. Raw reads advantage of the richer millieux offered by the hepatobiliary organs. Protease families differ- from F. hepatica have been deposited in the entially expanded between diverse trematodes may facilitate migration and survival within GenBank sequence read archive (SRA), as the heterogeneous environments and niches within the mammalian host. Surprisingly, the BioProject PRJNA179522. Raw RNAseq reads from F. hepatica were submitted to the GenBank sequencing of Oregon and Uruguay F. hepatica isolates led to the first discovery of an endo- sequence read archive (SRA) under the same bacteria in this species. Two contigs from the F. hepatica Oregon assembly were joined to BioProject id, with the following accession complete the 859,205 bp genome of a novel Neorickettsia endobacterium (nFh) closely numbers: SRX1037419, SRX1037422, related to the etiological agents of human Sennetsu and Potomac horse fevers. Immunohis- SRX1037423, SRX1037421, SRX1037418. The F. hepatica Neorickettsia genome and predicted tochemical studies targeting a Neorickettsia surface protein found nFh in specific organs PLOS Genetics | DOI:10.1371/journal.pgen.1006537 January 6, 2017 1 / 25 The Liver Fluke Fasciola hepatica Carries the Endobacteria Neorickettsia features are available under accession RefSeq and tissues of the adult trematode including the female reproductive tract, eggs, the Mehlis' NZ_AGCN00000000.1. All other relevant data are gland, seminal vesicle, and oral suckers, suggesting putative routes for fluke-to-fluke and within the paper and its Supporting Information files. fluke-to-host transmission. The genomes of F. hepatica and nFh will serve as a resource for further exploration of the biology of F. hepatica, and specifically its newly discovered trans- Funding: Sequencing of the genomes of Fasciola/ Neorickettsia was supported by the `Sequencing kingdom interaction with nFh and the impact of both species on disease in ruminants and the etiological agents of the Food-Borne humans. Trematodiases' project (NIH-NHGRI award number U54HG003079). The Barnes Jewish Hospital Foundation supported the immunolocalization studies. The ComisioÂn Sectorial de InvestigacioÂn CientõÂfica (CSIC-UDELAR) financially supported the Author Summary Uruguayan co-authors. The funders had no role in study design, data collection and analysis, decision This report presents novel findings revealing (a) the genome sequence of the food-borne to publish, or preparation of the manuscript. trematode Fasciola hepatica (the liver fluke) isolated from sheep, which stands out among neglected tropical diseases due to its zoonotic impact on both human and animal health Competing Interests: The authors have declared that no competing interests exist. and (b) the first instance (and the genome) of the rickettsial endobacterium of the genus Neorickettsia in F. hepatica. Using stage-specific gene expression data, we identified liver fluke proteins likely involved in host-parasite interactions, and using immunolocalization, we confirmed Neorickettsia in organs and tissues of the adult trematode. The presence of the bacteria in fluke reproductive tissues and eggs suggests a possible mechanism for verti- cal transmission, and the presence of bacteria in the oral sucker used to anchor flukes to the lining of the biliary tract suggests a potential mechanism for horizontal transmission to the mammalian host. This is of interest because related Neorickettsia cause severe, even deadly, illness in a variety of species, including humans. This is the first report to localize Neorickettsia endobacteria within the tissues of adult F. hepatica. The discoveries in our manuscript have wide impact for the fields of both the pathophysiology and evolution of Fasciola and related FBTs, and the transmission strategies of Neorickettsia. Introduction Food borne trematodes (FBTs) are an assemblage of platyhelminth parasites that are transmit- ted through the food chain [1]. Among the four major groups of FBT infections recognized as neglected tropical diseases (NTDs) by the World Health Organization [2], fascioliasis stands out due to its zoonotic impact on both human and animal health [3]. Fasciola species are major pathogens of domesticated ruminants, but they infect numerous other species of mam- mals, including people [4]. Due to the significant burden to livestock globally, with annual losses exceeding US $3.2 billion [5] and public health with ~50 million infected people [4], these parasites are among the most-extensively studied FBTs. Like other digenetic trematodes, Fasciola hepatica has a complex developmental cycle [1]. The hermaphroditic adult stage resides in the host bile ducts and reproduces sexually, releasing thousands of eggs each day that pass with the bile into the intestines and exit in the fecal stream. Eggs that reach fresh water embryonate over a couple of weeks, hatching a free-swim- ming miracidium that seeks out and infects a snail of the family Lymnaeidae. Within the snail, the parasite progresses through sporocyst, redia, and daughter redia stages by asexual replica- tion and development, resulting in the release thousands of the cercariae [6]. The free-living, aquatic cercaria encysts as the metacercarial stage on solid substrates, including vegetation at the margins of the watercourse. When infected vegetation (for example, uncooked watercress) are ingested by a suitable host, the metacercaria excysts in the duodenum, transverses the wall of the small intestine, migrates through the peritoneal cavity, and penetrates the Glisson's PLOS Genetics | DOI:10.1371/journal.pgen.1006537 January 6, 2017 2 / 25 The Liver Fluke Fasciola hepatica Carries the Endobacteria Neorickettsia capsule of the liver [7]. The migration of the juvenile fluke though the liver parenchyma into the biliary ducts damages the liver and provokes reactions associated with the acute phase of the infection. This phase is accompanied by systemic disease including fever, nausea and abdominal pain. Once the adult is established in the bile ducts, anemia, inflammation, fibrosis, cholangitis and biliary stasis may ensue. In this chronic phase adult worms can survive several years in the absence of intervention [8, 9]. Despite its potent and broad action against other human parasitic flatworms the anthelmintic drug praziquantel has no effect on
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