Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1

Liina Kinkar, Teivi Laurimäe, Gerardo Acosta-Jamett, Vanessa Andresiuk, Ibrahim Balkaya, Adriano Casulli, Robin B. Gasser, Joke van der Giessen, Luis Miguel González, Karen L. Haag, Houria Zait, Malik Irshadullah, Abdul Jabbar, David J. Jenkins, Eshrat Beigom Kia, Maria Teresa Manfredi, Hossein Mirhendi, Selim M'rad, Mohammad Rostami-Nejad, Myriam Oudni-M'rad & 11 others Nora Beatriz Pierangeli, Francisco Ponce-Gordo, Steffen Rehbein, Mitra Sharbatkhori, Sami Simsek, Silvia Viviana Soriano, Hein Sprong, Viliam Šnábel, Gérald Umhang, Antonio Varcasia, Urmas Saarma

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Echinococcus granulosus sensu stricto (s.s.) is the major cause of human cystic echinococcosis worldwide and is listed among the most severe parasitic diseases of humans. To date, numerous studies have investigated the genetic diversity and population structure of E. granulosus s.s. in various geographic regions. However, there has been no global study. Recently, using mitochondrial DNA, it was shown that E. granulosus s.s. G1 and G3 are distinct genotypes, but a larger dataset is required to confirm the distinction of these genotypes. The objectives of this study were to: (i) investigate the distinction of genotypes G1 and G3 using a large global dataset; and (ii) analyse the genetic diversity and phylogeography of genotype G1 on a global scale using near-complete mitogenome sequences. For this study, 222 globally distributed E. granulosus s.s. samples were used, of which 212 belonged to genotype G1 and 10 to G3. Using a total sequence length of 11,682 bp, we inferred phylogenetic networks for three datasets: E. granulosus s.s. (n = 222), G1 (n = 212) and human G1 samples (n = 41). In addition, the Bayesian phylogenetic and phylogeographic analyses were performed. The latter yielded several strongly supported diffusion routes of genotype G1 originating from Turkey, Tunisia and Argentina. We conclude that: (i) using a considerably larger dataset than employed previously, E. granulosus s.s. G1 and G3 are indeed distinct mitochondrial genotypes; (ii) the genetic diversity of E. granulosus s.s. G1 is high globally, with lower values in South America; and (iii) the complex phylogeographic patterns emerging from the phylogenetic and geographic analyses suggest that the current distribution of genotype G1 has been shaped by intensive animal trade.
Original languageEnglish
Pages (from-to)729-742
Number of pages14
JournalInternational Journal for Parasitology
Volume48
Issue number9-10
Early online dateMay 2018
DOIs
Publication statusPublished - Aug 2018

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Phylogeography
Echinococcus granulosus
Cestoda
Zoonoses
Genotype
Tunisia
Parasitic Diseases
South America
Echinococcosis
Argentina
Turkey
Mitochondrial DNA
Datasets

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Kinkar, Liina ; Laurimäe, Teivi ; Acosta-Jamett, Gerardo ; Andresiuk, Vanessa ; Balkaya, Ibrahim ; Casulli, Adriano ; Gasser, Robin B. ; van der Giessen, Joke ; González, Luis Miguel ; Haag, Karen L. ; Zait, Houria ; Irshadullah, Malik ; Jabbar, Abdul ; Jenkins, David J. ; Kia, Eshrat Beigom ; Manfredi, Maria Teresa ; Mirhendi, Hossein ; M'rad, Selim ; Rostami-Nejad, Mohammad ; Oudni-M'rad, Myriam ; Pierangeli, Nora Beatriz ; Ponce-Gordo, Francisco ; Rehbein, Steffen ; Sharbatkhori, Mitra ; Simsek, Sami ; Soriano, Silvia Viviana ; Sprong, Hein ; Šnábel, Viliam ; Umhang, Gérald ; Varcasia, Antonio ; Saarma, Urmas. / Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. In: International Journal for Parasitology. 2018 ; Vol. 48, No. 9-10. pp. 729-742.
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title = "Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1",
abstract = "Echinococcus granulosus sensu stricto (s.s.) is the major cause of human cystic echinococcosis worldwide and is listed among the most severe parasitic diseases of humans. To date, numerous studies have investigated the genetic diversity and population structure of E. granulosus s.s. in various geographic regions. However, there has been no global study. Recently, using mitochondrial DNA, it was shown that E. granulosus s.s. G1 and G3 are distinct genotypes, but a larger dataset is required to confirm the distinction of these genotypes. The objectives of this study were to: (i) investigate the distinction of genotypes G1 and G3 using a large global dataset; and (ii) analyse the genetic diversity and phylogeography of genotype G1 on a global scale using near-complete mitogenome sequences. For this study, 222 globally distributed E. granulosus s.s. samples were used, of which 212 belonged to genotype G1 and 10 to G3. Using a total sequence length of 11,682 bp, we inferred phylogenetic networks for three datasets: E. granulosus s.s. (n = 222), G1 (n = 212) and human G1 samples (n = 41). In addition, the Bayesian phylogenetic and phylogeographic analyses were performed. The latter yielded several strongly supported diffusion routes of genotype G1 originating from Turkey, Tunisia and Argentina. We conclude that: (i) using a considerably larger dataset than employed previously, E. granulosus s.s. G1 and G3 are indeed distinct mitochondrial genotypes; (ii) the genetic diversity of E. granulosus s.s. G1 is high globally, with lower values in South America; and (iii) the complex phylogeographic patterns emerging from the phylogenetic and geographic analyses suggest that the current distribution of genotype G1 has been shaped by intensive animal trade.",
keywords = "Cystic echinococcosis, Echinococcus granulosus, Genetic variability, Global phylogeography, Livestock domestication, Mitochondrial genome",
author = "Liina Kinkar and Teivi Laurim{\"a}e and Gerardo Acosta-Jamett and Vanessa Andresiuk and Ibrahim Balkaya and Adriano Casulli and Gasser, {Robin B.} and {van der Giessen}, Joke and Gonz{\'a}lez, {Luis Miguel} and Haag, {Karen L.} and Houria Zait and Malik Irshadullah and Abdul Jabbar and Jenkins, {David J.} and Kia, {Eshrat Beigom} and Manfredi, {Maria Teresa} and Hossein Mirhendi and Selim M'rad and Mohammad Rostami-Nejad and Myriam Oudni-M'rad and Pierangeli, {Nora Beatriz} and Francisco Ponce-Gordo and Steffen Rehbein and Mitra Sharbatkhori and Sami Simsek and Soriano, {Silvia Viviana} and Hein Sprong and Viliam Šn{\'a}bel and G{\'e}rald Umhang and Antonio Varcasia and Urmas Saarma",
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Kinkar, L, Laurimäe, T, Acosta-Jamett, G, Andresiuk, V, Balkaya, I, Casulli, A, Gasser, RB, van der Giessen, J, González, LM, Haag, KL, Zait, H, Irshadullah, M, Jabbar, A, Jenkins, DJ, Kia, EB, Manfredi, MT, Mirhendi, H, M'rad, S, Rostami-Nejad, M, Oudni-M'rad, M, Pierangeli, NB, Ponce-Gordo, F, Rehbein, S, Sharbatkhori, M, Simsek, S, Soriano, SV, Sprong, H, Šnábel, V, Umhang, G, Varcasia, A & Saarma, U 2018, 'Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1', International Journal for Parasitology, vol. 48, no. 9-10, pp. 729-742. https://doi.org/10.1016/j.ijpara.2018.03.006

Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. / Kinkar, Liina; Laurimäe, Teivi; Acosta-Jamett, Gerardo; Andresiuk, Vanessa; Balkaya, Ibrahim; Casulli, Adriano; Gasser, Robin B.; van der Giessen, Joke; González, Luis Miguel; Haag, Karen L.; Zait, Houria; Irshadullah, Malik; Jabbar, Abdul; Jenkins, David J.; Kia, Eshrat Beigom; Manfredi, Maria Teresa; Mirhendi, Hossein; M'rad, Selim; Rostami-Nejad, Mohammad; Oudni-M'rad, Myriam; Pierangeli, Nora Beatriz; Ponce-Gordo, Francisco; Rehbein, Steffen; Sharbatkhori, Mitra; Simsek, Sami; Soriano, Silvia Viviana; Sprong, Hein; Šnábel, Viliam; Umhang, Gérald; Varcasia, Antonio; Saarma, Urmas.

In: International Journal for Parasitology, Vol. 48, No. 9-10, 08.2018, p. 729-742.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1

AU - Kinkar, Liina

AU - Laurimäe, Teivi

AU - Acosta-Jamett, Gerardo

AU - Andresiuk, Vanessa

AU - Balkaya, Ibrahim

AU - Casulli, Adriano

AU - Gasser, Robin B.

AU - van der Giessen, Joke

AU - González, Luis Miguel

AU - Haag, Karen L.

AU - Zait, Houria

AU - Irshadullah, Malik

AU - Jabbar, Abdul

AU - Jenkins, David J.

AU - Kia, Eshrat Beigom

AU - Manfredi, Maria Teresa

AU - Mirhendi, Hossein

AU - M'rad, Selim

AU - Rostami-Nejad, Mohammad

AU - Oudni-M'rad, Myriam

AU - Pierangeli, Nora Beatriz

AU - Ponce-Gordo, Francisco

AU - Rehbein, Steffen

AU - Sharbatkhori, Mitra

AU - Simsek, Sami

AU - Soriano, Silvia Viviana

AU - Sprong, Hein

AU - Šnábel, Viliam

AU - Umhang, Gérald

AU - Varcasia, Antonio

AU - Saarma, Urmas

PY - 2018/8

Y1 - 2018/8

N2 - Echinococcus granulosus sensu stricto (s.s.) is the major cause of human cystic echinococcosis worldwide and is listed among the most severe parasitic diseases of humans. To date, numerous studies have investigated the genetic diversity and population structure of E. granulosus s.s. in various geographic regions. However, there has been no global study. Recently, using mitochondrial DNA, it was shown that E. granulosus s.s. G1 and G3 are distinct genotypes, but a larger dataset is required to confirm the distinction of these genotypes. The objectives of this study were to: (i) investigate the distinction of genotypes G1 and G3 using a large global dataset; and (ii) analyse the genetic diversity and phylogeography of genotype G1 on a global scale using near-complete mitogenome sequences. For this study, 222 globally distributed E. granulosus s.s. samples were used, of which 212 belonged to genotype G1 and 10 to G3. Using a total sequence length of 11,682 bp, we inferred phylogenetic networks for three datasets: E. granulosus s.s. (n = 222), G1 (n = 212) and human G1 samples (n = 41). In addition, the Bayesian phylogenetic and phylogeographic analyses were performed. The latter yielded several strongly supported diffusion routes of genotype G1 originating from Turkey, Tunisia and Argentina. We conclude that: (i) using a considerably larger dataset than employed previously, E. granulosus s.s. G1 and G3 are indeed distinct mitochondrial genotypes; (ii) the genetic diversity of E. granulosus s.s. G1 is high globally, with lower values in South America; and (iii) the complex phylogeographic patterns emerging from the phylogenetic and geographic analyses suggest that the current distribution of genotype G1 has been shaped by intensive animal trade.

AB - Echinococcus granulosus sensu stricto (s.s.) is the major cause of human cystic echinococcosis worldwide and is listed among the most severe parasitic diseases of humans. To date, numerous studies have investigated the genetic diversity and population structure of E. granulosus s.s. in various geographic regions. However, there has been no global study. Recently, using mitochondrial DNA, it was shown that E. granulosus s.s. G1 and G3 are distinct genotypes, but a larger dataset is required to confirm the distinction of these genotypes. The objectives of this study were to: (i) investigate the distinction of genotypes G1 and G3 using a large global dataset; and (ii) analyse the genetic diversity and phylogeography of genotype G1 on a global scale using near-complete mitogenome sequences. For this study, 222 globally distributed E. granulosus s.s. samples were used, of which 212 belonged to genotype G1 and 10 to G3. Using a total sequence length of 11,682 bp, we inferred phylogenetic networks for three datasets: E. granulosus s.s. (n = 222), G1 (n = 212) and human G1 samples (n = 41). In addition, the Bayesian phylogenetic and phylogeographic analyses were performed. The latter yielded several strongly supported diffusion routes of genotype G1 originating from Turkey, Tunisia and Argentina. We conclude that: (i) using a considerably larger dataset than employed previously, E. granulosus s.s. G1 and G3 are indeed distinct mitochondrial genotypes; (ii) the genetic diversity of E. granulosus s.s. G1 is high globally, with lower values in South America; and (iii) the complex phylogeographic patterns emerging from the phylogenetic and geographic analyses suggest that the current distribution of genotype G1 has been shaped by intensive animal trade.

KW - Cystic echinococcosis

KW - Echinococcus granulosus

KW - Genetic variability

KW - Global phylogeography

KW - Livestock domestication

KW - Mitochondrial genome

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