The benefits of analysing complete mitochondrial genomes: Deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7

Teivi Laurimäe; Liina Kinkar; Thomas Romig; Rihab A Omer; Adriano Casulli; Gérald Umhang; Robin B Gasser; Abdul Jabbar; Mitra Sharbatkhori; Hossein Mirhendi; Francisco Ponce-Gordo; Lorena E Lazzarini; Silvia V Soriano; Antonio Varcasia; Mohammad Rostami Nejad; Vanessa Andresiuk; Pablo Maravilla; Luis Miguel González; Monika Dybicz; Jakub Gawor; Mindaugas Šarkūnas; Viliam Šnábel; Tetiana Kuzmina; Urmas Saarma

doi:10.1016/j.meegid.2018.06.016

The benefits of analysing complete mitochondrial genomes: Deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7

Infect Genet Evol. 2018 Oct:64:85-94. doi: 10.1016/j.meegid.2018.06.016. Epub 2018 Jun 12.

Authors

Teivi Laurimäe¹, Liina Kinkar¹, Thomas Romig², Rihab A Omer³, Adriano Casulli⁴, Gérald Umhang⁵, Robin B Gasser⁶, Abdul Jabbar⁶, Mitra Sharbatkhori⁷, Hossein Mirhendi⁸, Francisco Ponce-Gordo⁹, Lorena E Lazzarini¹⁰, Silvia V Soriano¹⁰, Antonio Varcasia¹¹, Mohammad Rostami Nejad¹², Vanessa Andresiuk¹³, Pablo Maravilla¹⁴, Luis Miguel González¹⁵, Monika Dybicz¹⁶, Jakub Gawor¹⁷, Mindaugas Šarkūnas¹⁸, Viliam Šnábel¹⁹, Tetiana Kuzmina²⁰, Urmas Saarma²¹

Affiliations

¹ Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003 Tartu, Estonia.
² Institute of Zoology, Parasitology Unit, University of Hohenheim, 70599 Stuttgart, Germany.
³ National University Research Institute, National University Sudan, Khartoum, Sudan.
⁴ World Health Organization Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis (in humans and animals), Istituto Superiore di Sanità, Viale Regina Elena 299, 00161 Rome, Italy; European Union Reference Laboratory for Parasites (EURLP), Istituto Superiore di Sanità, Viale Regina Elena 299, 00161 Rome, Italy.
⁵ Anses, Wildlife Surveillance and Eco-epidemiology Unit, National Reference Laboratory for Echinococcus spp., Nancy Laboratory for Rabies and Wildlife, 54220 Malzéville, France.
⁶ Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria 3010, Australia.
⁷ Laboratory Science Research Center, Golestan University of Medical Sciences, Gorgan, Iran.
⁸ Department of Parasitology and Mycology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran.
⁹ Department of Parasitology, Faculty of Pharmacy, Complutense University, Plaza Ramón y Cajal s/n, 28040 Madrid, Spain.
¹⁰ Department of Microbiology and Parasitology, Faculty of Medical Sciences, Comahue National University, Buenos Aires, 1400, 8300 Neuquén, Argentina.
¹¹ Laboratorio di Parassitologia e Malattie Parassitarie, Ospedale Didattico Veterinario Dipartimento di Medicina Veterinaria, Università degli Studi di Sassari, Via Vienna 2, 07100 Sassari, Italy.
¹² Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
¹³ Laboratorio de Zoonosis Parasitarias, FCEyN, UNMdP, Funes 3350, CP: 7600, Mar del Plata, Buenos Aires, Argentina.
¹⁴ Hospital General "Dr. Manuel Gea Gonzalez", Departamento de Ecologia de Agentes Patogenos, DF 14080, Mexico.
¹⁵ Parasitology Department, Centro Nacional de Microbiologia, Instituto de Salud Carlos III, Majadahonda, Madrid 28220, Spain.
¹⁶ Department of General Biology and Parasitology, 5 Chałubińskiego Str., 02-004 Warsaw, Medical University of Warsaw, Poland.
¹⁷ W. Stefański Institute of Parasitology, Polish Academy of Science, Twarda51/55, Warsaw 00-818, Poland.
¹⁸ Department of Veterinary Pathobiology, Veterinary Academy, Lithuanian University of Health Sciences, Tilžes Street 18, 47181 Kaunas, Lithuania.
¹⁹ Institute of Parasitology, Slovak Academy of Sciences, Košice, Hlinkova 3, 040 01 Košice, Slovakia.
²⁰ I.I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, 01030 Kyiv, Ukraine.
²¹ Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003 Tartu, Estonia. Electronic address: Urmas.Saarma@ut.ee.

PMID: 29906638
DOI: 10.1016/j.meegid.2018.06.016

Abstract

Cystic echinococcosis (CE) is a zoonotic disease caused by the larval stage of the species complex Echinococcus granulosus sensu lato. Within this complex, genotypes G6 and G7 have been frequently associated with human CE worldwide. Previous studies exploring the genetic variability and phylogeography of genotypes G6 and G7 have been based on relatively short mtDNA sequences, and the resolution of these studies has often been low. Moreover, using short sequences, the distinction between G6 and G7 has in some cases remained challenging. The aim here was to sequence complete mitochondrial genomes (mitogenomes) to obtain deeper insight into the genetic diversity, phylogeny and population structure of genotypes G6 and G7. We sequenced complete mitogenomes of 94 samples collected from 15 different countries worldwide. The results demonstrated that (i) genotypes G6 and G7 can be clearly distinguished when mitogenome sequences are used; (ii) G7 is represented by two major haplogroups, G7a and G7b, the latter being specific to islands of Corsica and Sardinia; (iii) intensive animal trade, but also geographical isolation, have likely had the largest impact on shaping the genetic structure and distribution of genotypes G6 and G7. In addition, we found phylogenetically highly divergent haplotype from Mongolia (Gmon), which had a higher affinity to G6.

Keywords: Cystic echinococcosis; Genotype G6; Genotype G7; Hydatid disease; Mitochondrial genome; Zoonosis.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bayes Theorem
Echinococcus granulosus / genetics*
Genetic Variation
Genetics, Population
Genome, Mitochondrial*
Genomics* / methods
Genotype*
Geography
Haplotypes
Phylogeny*
Phylogeography