Mitogenomics and Evolutionary History of Rodent Whipworms (Trichuris spp.) Originating from Three Biogeographic Regions
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
18-19629S
Grantová Agentura České Republiky
PubMed
34207698
PubMed Central
PMC8228637
DOI
10.3390/life11060540
PII: life11060540
Knihovny.cz E-zdroje
- Klíčová slova
- Afrotropical, Indomalayan, Trichuris, comparative genomics, mitogenomes, palearctic, phylogenetics, rodents, whipworms,
- Publikační typ
- časopisecké články MeSH
Trichuris spp. is a widespread nematode which parasitizes a wide range of mammalian hosts including rodents, the most diverse mammalian order. However, genetic data on rodent whipworms are still scarce, with only one published whole genome (Trichuris muris) despite an increasing demand for whole genome data. We sequenced the whipworm mitogenomes from seven rodent hosts belonging to three biogeographic regions (Palearctic, Afrotropical, and Indomalayan), including three previously described species: Trichuris cossoni, Trichurisarvicolae, and Trichurismastomysi. We assembled and annotated two complete and five almost complete mitogenomes (lacking only the long non-coding region) and performed comparative genomic and phylogenetic analyses. All the mitogenomes are circular, have the same organisation, and consist of 13 protein-coding, 2 rRNA, and 22 tRNA genes. The phylogenetic analysis supports geographical clustering of whipworm species and indicates that T. mastomysi found in Eastern Africa is able to infect multiple closely related rodent hosts. Our results are informative for species delimitation based on mitochondrial markers and could be further used in studies on phylogeny, phylogeography, and population genetics of rodent whipworms.
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Ghai R.R., Simons N.D., Chapman C.A., Omeja P.A., Davies T.J., Ting N., Goldberg T.L. Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non human primates in Uganda. PLoS Negl. Trop. Dis. 2014;8:e3256. doi: 10.1371/journal.pntd.0003256. PubMed DOI PMC
Wasimuddin J.B., Ribas A., Baird S.J., Piálek J., Goüy de Bellocq J. Testing parasite Intimacy: The whipworm Trichuris muris in the European house mouse hybrid zone. Ecol. Evol. 2016;6:2688–2701. doi: 10.1002/ece3.2022. PubMed DOI PMC
Fenwick A. The global burden of neglected tropical diseases. Public Health. 2012;126:233–236. doi: 10.1016/j.puhe.2011.11.015. PubMed DOI
Musser G., Carleton M. Superfamily Muroidea. In: Wilson D., Reeder D., editors. Mammal Species of the World. A Taxonomic and Geographic Reference. 3rd ed. Volume 2. Johns Hopkins University Press; Baltimore, MD, USA: 2005. pp. 894–1531.
Schenk J.J., Rowe K.C., Steppan S.J. Ecological opportunity and incumbency in the diversification of repeated continental colonizations by muroid rodents. Syst. Biol. 2013;62:837–864. doi: 10.1093/sysbio/syt050. PubMed DOI
Aghová T., Kimura Y., Bryja J., Dobigny G., Granjon L., Kergoat G.J. Fossils know it best: Using a new set of fossil calibrations to improve the temporal phylogenetic framework of murid rodents (Rodentia: Muridae) Mol. Phylogenet. Evol. 2018;128:98–111. doi: 10.1016/j.ympev.2018.07.017. PubMed DOI
Petružela J., Bryja J., Bryjová A., Katakweba A., Sabuni C., Baird S.J., Goüy de Bellocq J. Evolutionary history of Pneumocystis fungi in their African rodent hosts. Inf. Genet. Evol. 2019;75:103934. doi: 10.1016/j.meegid.2019.103934. PubMed DOI
Latinne A., Bezé F., Delhaes L., Pottier M., Gantois N., Nguyen J., Blasdell K., Dei-Cas E., Morand S., Chabé M. Genetic diversity and evolution of Pneumocystis fungi infecting wild Southeast Asian murid rodents. Parasitology. 2018;145:885–900. doi: 10.1017/S0031182017001883. PubMed DOI
Baird S.J., Ribas A., Macholán M., Albrecht T., Piálek J., Goüy de Bellocq J. Where are the wormy mice? A reexamination of hybrid parasitism in the European house mouse hybrid zone. Evolution. 2012;66:2757–2772. doi: 10.1111/j.1558-5646.2012.01633.x. PubMed DOI
Ribas A., López S., Makundi R.H., Leirs H., Goüy de Bellocq J. Trichuris spp. (Nematoda: Trichuridae) from two rodents, Mastomys natalensis and Gerbilliscus vicinus in Tanzania. J. Parasitol. 2013;99:868–875. doi: 10.1645/12-151.1. PubMed DOI
Brouat C., Duplantier J.M. Host habitat patchiness and the distance decay of similarity among gastro-intestinal nematode communities in two species of Mastomys (southeastern Senegal) Oecologia. 2007;152:715–720. doi: 10.1007/s00442-007-0680-8. PubMed DOI
Ribas A., Wells K., Morand S., Chaisiri K., Agatsuma T., Lakim M.B., Yuh Tuh F.Y., Saijuntha W. Whipworms of south-east Asian rodents are distinct from Trichuris muris. Parasitol. Int. 2020;77:102128. doi: 10.1016/j.parint.2020.102128. PubMed DOI
Glover M., Colombo S.A., Thornton D.J., Grencis R.K. Trickle infection and immunity to Trichuris muris. PLoS Pathog. 2019;15:e1007926. doi: 10.1371/journal.ppat.1007926. PubMed DOI PMC
Foth B.J., Tsai I.J., Reid A.J., Bancroft A.J., Nichol S., Tracey A., Holroyd N., Cotton J.A., Stanley E.J., Zarowiecki M., et al. Whipworm genome and dual-species transcriptome analyses provide molecular insights into an intimate host-parasite interaction. Nat. Genet. 2014;46:693–700. doi: 10.1038/ng.3010. PubMed DOI PMC
Jex A.R., Nejsum P., Schwarz E.M., Hu L., Young N.D., Hall R.S., Korhonen P.K., Liao S., Thamsborg S., Xia J., et al. Genome and transcriptome of the porcine whipworm Trichuris suis. Nat. Genet. 2014;46:701–706. doi: 10.1038/ng.3012. PubMed DOI PMC
Liu G.H., Wang Y., Xu M.J., Zhou D.H., Ye Y.G., Li J.Y., Song H.Q., Lin R.Q., Zhu X.Q. Characterization of the complete mitochondrial genomes of two whipworms Trichuris ovis and Trichuris discolor (Nematoda: Trichuridae) Inf. Genet. Evol. 2012;12:1635–1641. doi: 10.1016/j.meegid.2012.08.005. PubMed DOI
Hawash M.B., Andersen L.O., Gasser R.B., Stensvold C.R., Nejsum P. Mitochondrial genome analyses suggest multiple Trichuris species in humans, baboons, and pigs from different geographical regions. PLoS Neglect. Trop. Dis. 2015;9:e0004059. doi: 10.1371/journal.pntd.0004059. PubMed DOI PMC
Holroyd N., Kikuchi T., Berriman M. Genome, Transcriptome and Proteome Adaptations to Nematode Parasitism in Strongyloides, Direct Genbank Submission, NC_028621. [(accessed on 15 January 2021)];2020 Available online: https://www.ncbi.nlm.nih.gov/nucleotide/NC_028621.1.
Jex A.R., Waeschenbach A., Hu M., Van Wyk J.A., Beveridge I., Littlewood D.T.J., Gasser R.B. The mitochondrial genomes of Ancylostoma caninum and Bunostomum phlebotomum—Two hookworms of animal health and zoonotic importance. BMC Genom. 2009;10:79. doi: 10.1186/1471-2164-10-79. PubMed DOI PMC
Hu M., Chilton N.B., Gasser R.B. The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea) Int. J. Parasitol. 2002;32:145–158. doi: 10.1016/S0020-7519(01)00316-2. PubMed DOI
Li M.W., Lin R.Q., Song H.Q., Wu X.Y., Zhu X.Q. The complete mitochondrial genomes for three Toxocara species of human and animal health significance. BMC Genom. 2008;9:224. doi: 10.1186/1471-2164-9-224. PubMed DOI PMC
Kern E., Kim T., Park J.K. The mitochondrial genome in nematode phylogenetics. Front. Ecol. Evol. 2020;8:250. doi: 10.3389/fevo.2020.00250. DOI
Cutillas C., Callejon R., De Rojas M., Tewes B., Ubeda J.M., Ariza C., Guevara D.C. Trichuris suis and Trichuris trichiura are different nematode species. Acta Trop. 2009;111:299–307. doi: 10.1016/j.actatropica.2009.05.011. PubMed DOI
Feliu C., Spakulová M., Casanova J.C., Renaud F., Morand S., Hugot J.P., Santala P., Durand P. Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: Characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae) J. Parasitol. 2000;86:442–449. doi: 10.1645/0022-3395(2000)086[0442:GAMHIS]2.0.CO;2. PubMed DOI
Eberhardt A.T., del Rosario Robles M., Monje L.D., Beldomenico P.M., Callejón R. A new Trichuris species (Nematoda: Trichuridae) from capybaras: Morphological-molecular characterization and phylogenetic relationships. Acta Trop. 2019;190:244–252. doi: 10.1016/j.actatropica.2018.11.029. PubMed DOI
Callejón R., Cutillas C., Nadler S.A. Nuclear and mitochondrial genes for inferring Trichuris phylogeny. Parasitol. Res. 2015;114:4591–4599. doi: 10.1007/s00436-015-4705-7. PubMed DOI
Rivero J., Callejón R., Cutillas C. Complete Mitochondrial Genome of Trichuris trichiura from Macaca sylvanus and Papio papio. Life. 2021;11:126. doi: 10.3390/life11020126. PubMed DOI PMC
Verster A. Trichuris species from South African rodents and a hyracoid. Onderstepoort J. Vet. Res. 1960;28:465–471.
Těšíková J., Bryjová A., Bryja J., Lavrenchenko L.A., Goüy de Bellocq J. Hantavirus strains in East Africa related to Western African hantaviruses. Vector-Borne Zoonot Dis. 2017;17:278–280. doi: 10.1089/vbz.2016.2022. PubMed DOI
Lecompte É., Granjon L., Peterhans J.K., Denys C. Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): A new African radiation? Comptes Rendus Biol. 2002;325:827–840. doi: 10.1016/S1631-0691(02)01488-9. PubMed DOI
Cuypers L.N., Baird S.J., Hánová A., Locus T., Katakweba A.S., Gryseels S., Bryja J., Leirs H., Goüy de Bellocq J. Three arenaviruses in three subspecific natal multimammate mouse taxa in Tanzania: Same host specificity, but different spatial genetic structure? Virus Evol. 2020;6:veaa039. doi: 10.1093/ve/veaa039. PubMed DOI PMC
Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data, Babraham Bioinformatics. [(accessed on 15 January 2021)];2010 Available online: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Jiang H., Lei R., Ding S.W., Zhu S. Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinform. 2014;15:182. doi: 10.1186/1471-2105-15-182. PubMed DOI PMC
Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
Buchfink B., Xie C., Huson D.H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods. 2015;12:59–60. doi: 10.1038/nmeth.3176. PubMed DOI
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Laetsch D.R., Blaxter M.L. BlobTools: Interrogation of genome assemblies. F1000Research. 2017;6:1287. doi: 10.12688/f1000research.12232.1. DOI
Darling A.C.E., Mau B., Blattner F.R., Perna N.T. Mauve: Multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394–1403. doi: 10.1101/gr.2289704. PubMed DOI PMC
Laslett D., Canbäck B. ARWEN: A program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics. 2008;24:172–175. doi: 10.1093/bioinformatics/btm573. PubMed DOI
Bernt M., Donath A., Jühling F., Externbrink F., Florentz C., Fritzsch G., Pütz J., Middendorf M., Stadler P.F. MITOS: Improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 2013;69:313–319. doi: 10.1016/j.ympev.2012.08.023. PubMed DOI
Python Software Foundation Python Language Reference, Version 3.6. [(accessed on 15 January 2021)]; Available online: http://www.python.org.
Cock P.J., Antao T., Chang J.T., Chapman B.A., Cox C.J., Dalke A., Friedgerg I., Hamelryck T., Kauff F., Wilczynski B., et al. Biopython: Freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics. 2009;25:1422–1423. doi: 10.1093/bioinformatics/btp163. PubMed DOI PMC
Harris C.R., Millman K.J., van der Walt S.J., Gommers R., Virtanen P., Cournapeau D., Wieser E., Taylor J., Berg S., Smith N.J., et al. Array programming with NumPy. Nature. 2020;585:357–362. doi: 10.1038/s41586-020-2649-2. PubMed DOI PMC
Hunter J.D. Matplotlib: A 2D graphics environment. IEEE Ann. Hist. Comput. 2007;9:90–95. doi: 10.1109/MCSE.2007.55. DOI
Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods. 2012;9:772. doi: 10.1038/nmeth.2109. PubMed DOI PMC
Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC
Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC
Steppan S.J., Schenk J.J. Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS ONE. 2017;12:e0183070. doi: 10.1371/journal.pone.0183070. PubMed DOI PMC
Zarlenga D.S., Rosenthal B.M., La Rosa G., Pozio E., Hoberg E.P. Post-Miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella. Proc. Natl. Acad. Sci. USA. 2006;103:7354–7359. doi: 10.1073/pnas.0602466103. PubMed DOI PMC
Mitreva M., Jasmer D.P., Zarlenga D.S., Wang Z., Abubucker S., Martin J., Taylor C.M., Yin Y., Fulton L., Minx P., et al. The draft genome of the parasitic nematode Trichinella spiralis. Nat. Genet. 2011;43:228–235. doi: 10.1038/ng.769. PubMed DOI PMC
Blouin M.S. Molecular prospecting for cryptic species of nematodes: Mitochondrial DNA versus internal transcribed spacer. Int. J. Parasitol. 2002;32:527–531. doi: 10.1016/S0020-7519(01)00357-5. PubMed DOI
Callejón R., de Rojas M., Nieberding C., Foronda P., Feliú C., Guevara D., Cutillas C. Molecular evolution of Trichuris muris isolated from different Muridae hosts in Europe. Parasitol. Res. 2010;107:631–641. doi: 10.1007/s00436-010-1908-9. PubMed DOI
Ribas A., Diagne C., Tatard C., Diallo M., Poonlaphdecha S., Brouat C. Whipworm diversity in West African rodents: A molecular approach and the description of Trichuris duplantieri n. sp.(Nematoda: Trichuridae) Parasitol. Res. 2017;116:1265–1271. doi: 10.1007/s00436-017-5404-3. PubMed DOI