Assembly and phylogeographical analysis of novel Taenia solium mitochondrial genomes suggest stratification within the African-American genotype.
Cysticercosis
Evolution
Genetics
Genomics
Haplotypes
Mitochondrial genome
Molecular epidemiology
Phylogenetics
Phylogeography
Taeniasis
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
06 Oct 2023
06 Oct 2023
Historique:
received:
14
02
2023
accepted:
30
08
2023
medline:
9
10
2023
pubmed:
7
10
2023
entrez:
6
10
2023
Statut:
epublish
Résumé
Taenia solium is a parasite of public health concern, causing human taeniasis and cysticercosis. Two main genotypes have been identified: Asian and African-American. Although characterizing T. solium genotypes is crucial to understanding the genetic epidemiology of its diseases, not much is known about the differences between T. solium mitochondrial genomes from different genotypes. Also, little is known about whether genotypes are further subdivided. Therefore, this study aimed to identify a set of point mutations distributed throughout the T. solium mitochondrial genome that differentiate the African-American from the Asian genotype. Another objective was to identify whether T. solium main genotypes are further stratified. One Mexican and two Peruvian T. solium mitochondrial genomes were assembled using reads available in the NCBI Sequence Read Archive and the reference genome from China as a template. Mutations with respect to the Chinese reference were identified by multiple genome alignment. Jensen-Shannon and Grantham scores were computed for mutations in protein-coding genes to evaluate whether they affected protein function. Phylogenies by Bayesian inference and haplotype networks were constructed using cytochrome c oxidase subunit 1 and cytochrome b from these genomes and other isolates to infer phylogeographical relationships. A set of 31 novel non-synonymous point mutations present in all genomes of the African-American genotype were identified. These mutations were distributed across the mitochondrial genome, differentiating the African-American from the Asian genotype. All occurred in non-conserved protein positions. Furthermore, the analysis suggested a stratification of the African-American genotypes into an East African and a West African sublineage. A novel set of 31 non-synonymous mutations differentiating the main T. solium genotypes was identified. None of these seem to be causing differences in mitochondrial protein function between parasites of the two genotypes. Furthermore, two sublineages within the African-American genotype are proposed for the first time. The presence of the East African sublineage in the Americas suggests an underestimated connection between East African and Latin American countries that might have arisen in the major slave trade between Portuguese Mozambique and the Americas. The results obtained here help to complete the molecular epidemiology of the parasite.
Sections du résumé
BACKGROUND
BACKGROUND
Taenia solium is a parasite of public health concern, causing human taeniasis and cysticercosis. Two main genotypes have been identified: Asian and African-American. Although characterizing T. solium genotypes is crucial to understanding the genetic epidemiology of its diseases, not much is known about the differences between T. solium mitochondrial genomes from different genotypes. Also, little is known about whether genotypes are further subdivided. Therefore, this study aimed to identify a set of point mutations distributed throughout the T. solium mitochondrial genome that differentiate the African-American from the Asian genotype. Another objective was to identify whether T. solium main genotypes are further stratified.
METHODS
METHODS
One Mexican and two Peruvian T. solium mitochondrial genomes were assembled using reads available in the NCBI Sequence Read Archive and the reference genome from China as a template. Mutations with respect to the Chinese reference were identified by multiple genome alignment. Jensen-Shannon and Grantham scores were computed for mutations in protein-coding genes to evaluate whether they affected protein function. Phylogenies by Bayesian inference and haplotype networks were constructed using cytochrome c oxidase subunit 1 and cytochrome b from these genomes and other isolates to infer phylogeographical relationships.
RESULTS
RESULTS
A set of 31 novel non-synonymous point mutations present in all genomes of the African-American genotype were identified. These mutations were distributed across the mitochondrial genome, differentiating the African-American from the Asian genotype. All occurred in non-conserved protein positions. Furthermore, the analysis suggested a stratification of the African-American genotypes into an East African and a West African sublineage.
CONCLUSIONS
CONCLUSIONS
A novel set of 31 non-synonymous mutations differentiating the main T. solium genotypes was identified. None of these seem to be causing differences in mitochondrial protein function between parasites of the two genotypes. Furthermore, two sublineages within the African-American genotype are proposed for the first time. The presence of the East African sublineage in the Americas suggests an underestimated connection between East African and Latin American countries that might have arisen in the major slave trade between Portuguese Mozambique and the Americas. The results obtained here help to complete the molecular epidemiology of the parasite.
Identifiants
pubmed: 37803424
doi: 10.1186/s13071-023-05958-z
pii: 10.1186/s13071-023-05958-z
pmc: PMC10559519
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
349Subventions
Organisme : NIH HHS
ID : U19AI129909
Pays : United States
Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Yoshino K. Studies on the post-embryonal development of Taenia solium Part I. On the hatching of the eggs of Taenia solium. J Formos Med Assoc. 1933;32:1392–409.
Yoshino K. Studies on the postembryonal development of Taenia solium. Part II. On the youngest form of Cysticercus cellulosae and on the migratory course of the Oncosphaera of Taenia solium within the intermediate host. J Formos Med Assoc. 1933;32:1569–86.
Yoshino K. Studies on the postembryonal development of Taenia solium. Part III. On the development of Cysticercus cellulosae within the definite intermediate host. J Formos Med Assoc. 1933;32:166–9.
Singh G, Burneo JG, Sander JW. From seizures to epilepsy and its substrates: Neurocysticercosis. Epilepsia. 2013;54:783–92.
pubmed: 23621876
Nakao M, Okamoto M, Sako Y, Yamasaki H, Nakaya K, Ito A. A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology. 2002;124:657–62.
pubmed: 12118722
Martinez-Hernandez F, Jimenez-Gonzalez DE, Chenillo P, Alonso-Fernandez C, Maravilla P, Flisser A. Geographical widespread of two lineages of Taenia solium due to human migrations: can population genetic analysis strengthen this hypothesis? Infect Genet Evol. 2009;9:1108–14.
pubmed: 19778639
WHO. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015. Geneva: WHO Executive Summary; 2015.
Solano D, Navarro JC, León-Reyes A, Benítez-Ortiz W, Rodríguez-Hidalgo R. Molecular analyses reveal two geographic and genetic lineages for tapeworms, Taenia solium and Taenia saginata, from Ecuador using mitochondrial DNA. Exp Parasitol. 2016;171:49–56.
pubmed: 27769720
Michelet L, Carod J-F, Rakontondrazaka M, Ma L, Gay F, Dauga C. The pig tapeworm Taenia solium, the cause of cysticercosis: biogeographic (temporal and spacial) origins in Madagascar. Mol Phylogenet Evol. 2010;55:744–50.
pubmed: 20093191
Yanagida T, Carod J-F, Sako Y, Nakao M, Hoberg EP, Ito A. Genetics of the pig tapeworm in Madagascar reveal a history of human dispersal and colonization. PLoS ONE. 2014;9:e109002.
pubmed: 25329310
pmcid: 4198324
Michelet L, Dauga C. Molecular evidence of host influences on the evolution and spread of human tapeworms. Biol Rev. 2012;87:731–41.
pubmed: 22321512
Yanagida T, Swastika K, Dharmawan NS, Sako Y, Wandra T, Ito A, et al. Origin of the pork tapeworm Taenia solium in Bali and Papua, Indonesia. Parasitol Int. 2021;83:102285.
pubmed: 33486126
Hoberg EP, Alkire NL, Queiroz AD, Jones A. Out of Africa: origins of the Taenia tapeworms in humans. Proc R Soc Lond B Biol Sci. 2001;268:781–7.
Ito A, Budke CM. Genetic diversity of Taenia solium and its relation to clinical presentation of cysticercosis. Yale J Biol Med. 2021;94:343–9.
pubmed: 34211353
pmcid: 8223547
Campbell G, Garcia HH, Nakao M, Ito A, Craig PS. Genetic variation in Taenia solium. Parasitol Int. 2006;55:S121–6.
pubmed: 16352464
Okamoto M, Nakao M, Sako Y, Ito A. Molecular variation of Taenia solium in the world. Southeast Asian J Trop Med. 2001;32:90–3.
Nakao M, Sako Y, Ito A. The mitochondrial genome of the tapeworm Taenia solium: a finding of the abbreviated stop codon U. J Parasitol. 2003;89:633–5.
pubmed: 12880275
Sadlowski H, Schmidt V, Hiss J, Kuehn JA, Schneider CG, Zulu G, et al. Diagnosis of Taenia solium infections based on “mail order” RNA-sequencing of single tapeworm egg isolates from stool samples. PLoS Negl Trop Dis. 2021;15:e0009787.
pubmed: 34890398
pmcid: 8694474
Pajuelo MJ, Eguiluz M, Dahlstrom E, Requena D, Guzmán F, Ramirez M, et al. Identification and characterization of microsatellite markers derived from the whole genome analysis of Taenia solium. PLoS Negl Trop Dis. 2015;9:e0004316.
pubmed: 26697878
pmcid: 4689449
Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394–403.
pubmed: 15231754
pmcid: 442156
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302.
pubmed: 29029172
Nakao M, Sako Y, Yokoyama N, Fukunaga M, Ito A. Mitochondrial genetic code in cestodes. Mol Biochem Parasitol. 2000;111:415–24.
pubmed: 11163447
Krzywinski M, Schein J, Birol İ, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19:1639–45.
pubmed: 19541911
pmcid: 2752132
Lavikainen A, Haukisalmi V, Lehtinen MJ, Henttonen H, Oksanen A, Meri S. A phylogeny of members of the family Taeniidae based on the mitochondrial cox1 and nad1 gene data. Parasitology. 2008;135:1457–67.
pubmed: 18937885
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019;47:W636–41.
pubmed: 30976793
pmcid: 6602479
Capra JA, Singh M. Predicting functionally important residues from sequence conservation. Bioinformatics. 2007;23:1875–82.
pubmed: 17519246
Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20:1160–6.
pubmed: 28968734
Kuraku S, Zmasek CM, Nishimura O, Katoh K. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 2013;41:W22–8.
pubmed: 23677614
pmcid: 3692103
Grantham R. Amino acid difference formula to help explain protein evolution. Science. 1974;185:862–4.
pubmed: 4843792
Tavtigian S, Greenblatt MS, Lesueur F, Byrnes GB, IARC Unclassified Genetic Variants Working Group. In silico analysis of missense substitutions using sequence-alignment based methods. Hum Mutat. 2008;29:1327–36.
pubmed: 18951440
pmcid: 3431198
Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.
pubmed: 10742046
Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–77.
pubmed: 17654362
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.
pubmed: 24451623
pmcid: 3998144
Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214.
pubmed: 17996036
pmcid: 2247476
Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE). New York: IEEE; 2010. p. 1–8.
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772–772.
pubmed: 22847109
pmcid: 4594756
Bandelt HJ, Forster P, Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16:37–48.
pubmed: 10331250
Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.
pubmed: 21565059
Kinkar L, Korhonen PK, Cai H, Gauci CG, Lightowlers MW, Saarma U, et al. Long-read sequencing reveals a 4.4 kb tandem repeat region in the mitogenome of Echinococcus granulosus (sensu stricto) genotype G1. Parasit Vectors. 2019;12:238.
pubmed: 31097022
pmcid: 6521400
Baradaran R, Berrisford JM, Minhas GS, Sazanov LA. Crystal structure of the entire respiratory complex I. Nature. 2013;494:443–8.
pubmed: 23417064
pmcid: 3672946
Parey K, Haapanen O, Sharma V, Köfeler H, Züllig T, Prinz S, et al. High-resolution cryo-EM structures of respiratory complex I: mechanism, assembly, and disease. Sci Adv. 2019;5:1–11.
Cabrera-Orefice A, Yoga EG, Wirth C, Siegmund K, Zwicker K, Guerrero-Castillo S, et al. Locking loop movement in the ubiquinone pocket of complex I disengages the proton pumps. Nat Commun. 2018;9:4500.
pubmed: 30374105
pmcid: 6206036
Yanagida T, Sako Y, Nakao M, Nakaya K, Ito A. Taeniasis and cysticercosis due to Taenia solium in Japan. Parasit Vectors. 2012;5:18.
pubmed: 22248435
pmcid: 3398336
Hotomo AW, Theodorus D, Veriswan I. Neurocysticercosis (NCC) in 15-year-old girl, East Nusa Tenggara, Indonesia: a case report. Am J Pediatr. 2021;7:39.
Sutisna P, Kapti IN, Wandra T, Dharmawan NS, Swastika K, Raka Sudewi AA, et al. Towards a cysticercosis-free tropical resort island: a historical overview of taeniasis/cysticercosis in Bali. Acta Trop. 2019;190:273–83.
pubmed: 30385216
Pereira L, Macaulay V, Torroni A, Scozzari R, Prata MJ, Amorim A. Prehistoric and historic traces in the mtDNA of Mozambique: insights into the Bantu expansions and the slave trade. Ann Hum Genet. 2001;65:439–58.
pubmed: 11806853
Bowser F. The African slave in colonial Peru, 1524–1650. Standford, California: Standford University Press; 1974.