Phylogeography, Genetic Diversity and Population Structure of Echinococcus granulosus Sensu Stricto Inferred by Mitochondrial DNA Markers between Southeast of Iran and Pakistan
-
Davood Anvari
,
Shirzad Gholami
,
Adel Spotin
,
Seyed Abdollah Hosseini
,
Ahmad Daryani
,
Shahabeddin Sarvi
,
Mohammad Reza Narouei
,
Mona Hosseini
,
Abolghasem Siyadatpanah
Abstract
Background: Current study was designed to provide a better insight into the circulating genotypes, genetic diversity, and population structure of Echinococcus spp. between southeast of Iran and Pakistan.
Methods: From Jun 2020 to Dec 2020, 46 hydatid cysts were taken from human (n: 6), camel (n: 10), goat (n: 10), cattle (n: 10) and sheep (n: 10) in various cities of Sistan and Baluchestan Province of Iran, located at the neighborhood of Pakistan. DNA samples were extracted, amplified, and subjected to sequence analysis of cox1 and nad1 genes. Results: The phylogeny inferred by the Maximum Likelihood algorithm indicated that G1 genotype (n: 19), G3 genotype (n: 14) and G6 genotype (n: 13) assigned into their specific clades. The diversity indices showed a moderate (nad1: Hd: 0.485) to high hap- lotype diversity (cox1: Hd: 0.867) of E. granulosus s.s. (G1/G3) and low nucleotide diver- sity. The negative value of Tajima’s D and Fu’s Fs test displayed deviation from neutrali- ty indicating a recent population expansion. A parsimonious network of the haplotypes of cox1 displayed star-like features in the overall population containing IR9/PAK1/G1, IR2/PAK2/G3 and IR18/G6 as the most common haplotypes. A pairwise fixation index (Fst) indicated that E. granulosus s.s. populations are genetically moderate differen- tiated between southeast of Iran and Pakistan. The extension of haplotypes PAK18/G1 (sheep) and PAK26/G1 (cattle) toward Iranian haplogroup revealed that there is dawn of Echinococcus flow due to a transfer of alleles between mentioned populations through transport of livestock or their domestication.
Conclusion: The current findings strengthen our knowledge concerning the evolution- ary paradigms of E. granulosus in southeastern borders of Iran and is effective in control- ling of hydatidosis.
1. Thompson RCA. The taxonomy, phylogeny and transmission of Echinococcus. Exp Parasitol. 2008;119(4):439-446.
2. Budke CM, Deplazes P, Torgerson PR. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis. 2006;12(2):296-303.
3. Romig T, Ebi D, Wassermann M. Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol. 2015;213(3-4):76-84.
4. Nakao M, McManus DP, Schantz PM, Craig PS, Ito A. A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology. 2007;134(Pt 5):713-722.
5. Gholami S, Behrestaghi LE, Sarvi S, Alizadeh A, Spotin A. First description of the emergence of Echinococcus ortleppi (G5 genotype) in sheep and goats in Iran. Parasitol Int. 2021; 83:102316.
6. Kinkar L, Laurimäe T, Sharbatkhori M, et al. New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infect Genet Evol. 2017;52:52-58.
7. Lymbery AJ. Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. Adv Parasitol. 2017;95:111-145.
8. Spotin A, Mahami-Oskouei M, Harandi MF, et al. Genetic variability of Echinococcus granulosus complex in various geographical populations of Iran inferred by mitochondrial DNA sequences. Acta Trop. 2017;165:10-16.
9. Thompson RCA, Jenkins DJ. Echinococcus as a model system: biology and epidemiology. Int J Parasitol. 2014;44(12):865-877.
10. Bakhtiar NM, Spotin A, Mahami-Oskouei M, Ahmadpour E, Rostami A. Recent advances on innate immune pathways related to host–parasite cross-talk in cystic and alveolar echinococcosis. Parasit Vectors. 2020;13(1):232.
11. Siyadatpanah A, Anvari D, Zeydi AE, et al. A systematic review and meta-analysis of the genetic characterization of human echinococcosis in Iran, an endemic country. Epidemiol Health. 2019; 41:e2019024.
12. Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992;54(2):165-173.
13. Mahami-Oskouei M, Kaseb-Yazdanparast A, Spotin A, et al. Gene flow for Echinococcus granulosus metapopulations determined by mitochondrial sequences: a reliable approach for reflecting epidemiological drift of parasite among neighboring countries. Exp Parasitol. 2016;171:77-83.
14. Spotin A, Boufana B, Ahmadpour E, et al. Assessment of the global pattern of genetic diversity in Echinococcus multilocularis inferred by mitochondrial DNA sequences. Vet Parasitol. 2018;262:30-41.
15. Casulli A, Interisano M, Sreter T, et al. Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol. 2012;12(2):377-383.
16. Mueller RL, Macey JR, Jaekel M, Wake DB, Boore JL. Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes. Proc Natl Acad Sci U S A. 2004;101(38):13820-5. |
17. Shariatzadeh SA, Spotin A, Gholami S, et al. The first morphometric and phylogenetic perspective on molecular epidemiology of Echinococcus granulosus sensu lato in stray dogs in a hyperendemic Middle East focus, northwestern Iran. Parasit Vectors. 2015;8:409.
18. Siyadatpanah A, Daryani A, Sarvi S, et al. Phylogeography and genetic diversity of human hydatidosis in bordering the caspian sea, northern Iran by focusing on Echinococcus granulosus sensu stricto complex. Iran J Public Health. 2020;49(9): 1758-1768.
19. Spotin A, Gholami S, Nasab AN, et al. Designing and conducting in silico analysis for identifying of Echinococcus spp. with discrimination of novel haplotypes: an approach to better understanding of parasite taxonomic. Parasitol Res. 2015;114(4):1503-1509.
20. Mahami-Oskouei M, Ghabouli-Mehrabani N, Miahipour A, et al. Genotypic characterization of Echinococcus granulosus isolates based on the mitochondrial cytochrome c oxidase 1 (cox1) gene in Northwest Iran. Trop Biomed. 2015;32(4):717-725.
21. Alvi MA, Ohiolei JA, Saqib M, et al. Echinococcus granulosus (sensu stricto)(G1, G3) and E. ortleppi (G5) in Pakistan: phylogeny, genetic diversity and population structural analysis based on mitochondrial DNA. Parasit Vectors. 2020;13(1):347.
22. Ali I, Panni MK, Iqbal A, Munir I, Ahmad S, Ali A. Molecular characterization of Echinococcus species in Khyber pakhtunkhwa, pakistan. Acta Scientiae Veterinariae. 2015;43: 1277.
23. Ehsan M, Akhter N, Bhutto B, Arijo A, Gadahi JA. Prevalence and genotypic characterization of bovine Echinococcus granulosus isolates by using cytochrome oxidase 1 (Co1) gene in Hyderabad, Pakistan. Vet Parasitol. 2017;239:80-85.
24. Latif AA, Tanveer A, Maqbool A, Siddiqi N, Kyaw-Tanner M, Traub RJ. Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Vet Parasitol. 2010;170(1-2):44-49.
25. Mehmood N, Muqaddas H, Arshad M, Ullah MI, Khan ZI. Comprehensive study based on mtDNA signature (nad1) providing insights on Echinococcus granulosus ss genotypes from Pakistan and potential role of buffalo-dog cycle. Infect Genet Evol. 2020;81:104271.
26. Anvari D, Pourmalek N, Rezaei S, et al. The global status and genetic characterization of hydatidosis in camels (Camelus dromedarius): a systematic literature review with metaanalysis based on published papers. Parasitology. 2021;148(3):259-273.
27. Hedayati Z, Daryani A, Sarvi S, et al. Molecular Genotyping of the Human Cystic Echinococcosis in Mazandaran Province, North of Iran. Iran J Parasitol. 2019;14(1):151–158.
28. Spotin A, Mahami-Oskouei M, Ahmadpour E, et al. Global assessment of genetic paradigms of Pvmdr1 mutations in chloroquine-resistant Plasmodium vivax isolates. Trans R Soc Trop Med Hyg. 2020;114(5):339-345.
29. Spotin A, Mahami-Oskouei M, Nami S. Assessment of the global paradigms of genetic variability in Strongyloides stercoralis infrapopulations determined by mitochondrial DNA sequences. Comp Immunol Microbiol Infect Dis. 2019;67:101354.
30. Sharbatkhori M, Harandi MF, Mirhendi H, Hajialilo E, Kia EB. Sequence analysis of cox 1 and nad 1 genes in Echinococcus granulosus G3 genotype in camels (Camelus dromedarius) from central Iran. Parasitol Res. 2011;108(3):521-527.
31. Bandelt HJ, Forster P, Röhl A. Medianjoining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1):37-48.
32. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19(18):2496-2497.
33. Spotin A, Karamat M, Mahami-Oskouei M, et al. Genetic variability and transcontinental sharing of Giardia duodenalis infrapopulations determined by glutamate dehydrogenase gene. Acta Trop. 2018;177:146-156.
34. Knapp J, Nakao M, Yanagida T, et al. Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Mol Phylogenet Evol. 2011;61(3):628-638.
35. Shen X, Wang H, Ren J, Tian M, Wang M. The mitochondrial genome of Euphausia superba (Prydz Bay)(Crustacea: Malacostraca: Euphausiacea) reveals a novel gene arrangement and potential molecular markers. Mol Biol Rep. 2010;37(2):771–784.
36. Wei S jun, Tang P, Zheng L hua, Shi M, Chen X xin. The complete mitochondrial genome of Evania appendigaster (Hymenoptera: Evaniidae) has low A+ T content and a long intergenic spacer between atp8 and atp6. Mol Biol Rep. 2010;37(4):1931–1942.
37. Prugnolle F, Liu H, de Meeûs T, Balloux F. Population genetics of complex life-cycle parasites: an illustration with trematodes. Int J Parasitol. 2005;35(3):255-263.
38. Yan N, Nie HM, Jiang ZR, et al. Genetic variability of Echinococcus granulosus from the Tibetan plateau inferred by mitochondrial DNA sequences. Vet Parasitol. 2013;196(1-2):179-183.
2. Budke CM, Deplazes P, Torgerson PR. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis. 2006;12(2):296-303.
3. Romig T, Ebi D, Wassermann M. Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol. 2015;213(3-4):76-84.
4. Nakao M, McManus DP, Schantz PM, Craig PS, Ito A. A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology. 2007;134(Pt 5):713-722.
5. Gholami S, Behrestaghi LE, Sarvi S, Alizadeh A, Spotin A. First description of the emergence of Echinococcus ortleppi (G5 genotype) in sheep and goats in Iran. Parasitol Int. 2021; 83:102316.
6. Kinkar L, Laurimäe T, Sharbatkhori M, et al. New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infect Genet Evol. 2017;52:52-58.
7. Lymbery AJ. Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. Adv Parasitol. 2017;95:111-145.
8. Spotin A, Mahami-Oskouei M, Harandi MF, et al. Genetic variability of Echinococcus granulosus complex in various geographical populations of Iran inferred by mitochondrial DNA sequences. Acta Trop. 2017;165:10-16.
9. Thompson RCA, Jenkins DJ. Echinococcus as a model system: biology and epidemiology. Int J Parasitol. 2014;44(12):865-877.
10. Bakhtiar NM, Spotin A, Mahami-Oskouei M, Ahmadpour E, Rostami A. Recent advances on innate immune pathways related to host–parasite cross-talk in cystic and alveolar echinococcosis. Parasit Vectors. 2020;13(1):232.
11. Siyadatpanah A, Anvari D, Zeydi AE, et al. A systematic review and meta-analysis of the genetic characterization of human echinococcosis in Iran, an endemic country. Epidemiol Health. 2019; 41:e2019024.
12. Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992;54(2):165-173.
13. Mahami-Oskouei M, Kaseb-Yazdanparast A, Spotin A, et al. Gene flow for Echinococcus granulosus metapopulations determined by mitochondrial sequences: a reliable approach for reflecting epidemiological drift of parasite among neighboring countries. Exp Parasitol. 2016;171:77-83.
14. Spotin A, Boufana B, Ahmadpour E, et al. Assessment of the global pattern of genetic diversity in Echinococcus multilocularis inferred by mitochondrial DNA sequences. Vet Parasitol. 2018;262:30-41.
15. Casulli A, Interisano M, Sreter T, et al. Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol. 2012;12(2):377-383.
16. Mueller RL, Macey JR, Jaekel M, Wake DB, Boore JL. Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes. Proc Natl Acad Sci U S A. 2004;101(38):13820-5. |
17. Shariatzadeh SA, Spotin A, Gholami S, et al. The first morphometric and phylogenetic perspective on molecular epidemiology of Echinococcus granulosus sensu lato in stray dogs in a hyperendemic Middle East focus, northwestern Iran. Parasit Vectors. 2015;8:409.
18. Siyadatpanah A, Daryani A, Sarvi S, et al. Phylogeography and genetic diversity of human hydatidosis in bordering the caspian sea, northern Iran by focusing on Echinococcus granulosus sensu stricto complex. Iran J Public Health. 2020;49(9): 1758-1768.
19. Spotin A, Gholami S, Nasab AN, et al. Designing and conducting in silico analysis for identifying of Echinococcus spp. with discrimination of novel haplotypes: an approach to better understanding of parasite taxonomic. Parasitol Res. 2015;114(4):1503-1509.
20. Mahami-Oskouei M, Ghabouli-Mehrabani N, Miahipour A, et al. Genotypic characterization of Echinococcus granulosus isolates based on the mitochondrial cytochrome c oxidase 1 (cox1) gene in Northwest Iran. Trop Biomed. 2015;32(4):717-725.
21. Alvi MA, Ohiolei JA, Saqib M, et al. Echinococcus granulosus (sensu stricto)(G1, G3) and E. ortleppi (G5) in Pakistan: phylogeny, genetic diversity and population structural analysis based on mitochondrial DNA. Parasit Vectors. 2020;13(1):347.
22. Ali I, Panni MK, Iqbal A, Munir I, Ahmad S, Ali A. Molecular characterization of Echinococcus species in Khyber pakhtunkhwa, pakistan. Acta Scientiae Veterinariae. 2015;43: 1277.
23. Ehsan M, Akhter N, Bhutto B, Arijo A, Gadahi JA. Prevalence and genotypic characterization of bovine Echinococcus granulosus isolates by using cytochrome oxidase 1 (Co1) gene in Hyderabad, Pakistan. Vet Parasitol. 2017;239:80-85.
24. Latif AA, Tanveer A, Maqbool A, Siddiqi N, Kyaw-Tanner M, Traub RJ. Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Vet Parasitol. 2010;170(1-2):44-49.
25. Mehmood N, Muqaddas H, Arshad M, Ullah MI, Khan ZI. Comprehensive study based on mtDNA signature (nad1) providing insights on Echinococcus granulosus ss genotypes from Pakistan and potential role of buffalo-dog cycle. Infect Genet Evol. 2020;81:104271.
26. Anvari D, Pourmalek N, Rezaei S, et al. The global status and genetic characterization of hydatidosis in camels (Camelus dromedarius): a systematic literature review with metaanalysis based on published papers. Parasitology. 2021;148(3):259-273.
27. Hedayati Z, Daryani A, Sarvi S, et al. Molecular Genotyping of the Human Cystic Echinococcosis in Mazandaran Province, North of Iran. Iran J Parasitol. 2019;14(1):151–158.
28. Spotin A, Mahami-Oskouei M, Ahmadpour E, et al. Global assessment of genetic paradigms of Pvmdr1 mutations in chloroquine-resistant Plasmodium vivax isolates. Trans R Soc Trop Med Hyg. 2020;114(5):339-345.
29. Spotin A, Mahami-Oskouei M, Nami S. Assessment of the global paradigms of genetic variability in Strongyloides stercoralis infrapopulations determined by mitochondrial DNA sequences. Comp Immunol Microbiol Infect Dis. 2019;67:101354.
30. Sharbatkhori M, Harandi MF, Mirhendi H, Hajialilo E, Kia EB. Sequence analysis of cox 1 and nad 1 genes in Echinococcus granulosus G3 genotype in camels (Camelus dromedarius) from central Iran. Parasitol Res. 2011;108(3):521-527.
31. Bandelt HJ, Forster P, Röhl A. Medianjoining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1):37-48.
32. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19(18):2496-2497.
33. Spotin A, Karamat M, Mahami-Oskouei M, et al. Genetic variability and transcontinental sharing of Giardia duodenalis infrapopulations determined by glutamate dehydrogenase gene. Acta Trop. 2018;177:146-156.
34. Knapp J, Nakao M, Yanagida T, et al. Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Mol Phylogenet Evol. 2011;61(3):628-638.
35. Shen X, Wang H, Ren J, Tian M, Wang M. The mitochondrial genome of Euphausia superba (Prydz Bay)(Crustacea: Malacostraca: Euphausiacea) reveals a novel gene arrangement and potential molecular markers. Mol Biol Rep. 2010;37(2):771–784.
36. Wei S jun, Tang P, Zheng L hua, Shi M, Chen X xin. The complete mitochondrial genome of Evania appendigaster (Hymenoptera: Evaniidae) has low A+ T content and a long intergenic spacer between atp8 and atp6. Mol Biol Rep. 2010;37(4):1931–1942.
37. Prugnolle F, Liu H, de Meeûs T, Balloux F. Population genetics of complex life-cycle parasites: an illustration with trematodes. Int J Parasitol. 2005;35(3):255-263.
38. Yan N, Nie HM, Jiang ZR, et al. Genetic variability of Echinococcus granulosus from the Tibetan plateau inferred by mitochondrial DNA sequences. Vet Parasitol. 2013;196(1-2):179-183.
| Files | ||
| Issue | Vol 19 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i2.15850 | |
| Keywords | ||
| Echinococcus granulosus Haplotype diversity Mitochondrial DNA markers Phylogeny Iran | ||
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How to Cite
1.
Anvari D, Gholami S, Spotin A, Hosseini SA, Daryani A, Sarvi S, Narouei MR, Hosseini M, Siyadatpanah A. Phylogeography, Genetic Diversity and Population Structure of Echinococcus granulosus Sensu Stricto Inferred by Mitochondrial DNA Markers between Southeast of Iran and Pakistan. Iran J Parasitol. 2024;19(2):140-152.
