Genomic Variation among Strains of Crithidia bombi and C. expoeki
Jazyk angličtina Země Spojené státy americké Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
31511368
PubMed Central
PMC6739494
DOI
10.1128/msphere.00482-19
PII: 4/5/e00482-19
Knihovny.cz E-zdroje
- Klíčová slova
- Crithidia, Trypanosomatidae, genomics,
- MeSH
- Crithidia genetika MeSH
- fylogeneze MeSH
- genetická variace * MeSH
- genom protozoální * MeSH
- genomika MeSH
- interakce hostitele a parazita MeSH
- jednonukleotidový polymorfismus MeSH
- variabilita počtu kopií segmentů DNA * MeSH
- včely parazitologie MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Geografické názvy
- Aljaška MeSH
- Evropa MeSH
In this study, we sequenced and analyzed the genomes of 40 strains, in addition to the already-reported two type strains, of two Crithidia species infecting bumblebees in Alaska and Central Europe and demonstrated that different strains of Crithidia bombi and C. expoeki vary considerably in terms of single nucleotide polymorphisms and gene copy number. Based on the genomic structure, phylogenetic analyses, and the pattern of copy number variation, we confirmed the status of C. expoeki as a separate species. The Alaskan populations appear to be clearly separated from those of Central Europe. This pattern fits a scenario of rapid host-parasite coevolution, where the selective advantage of a given parasite strain is only temporary. This study provides helpful insights into possible scenarios of selection and diversification of trypanosomatid parasites.IMPORTANCE A group of trypanosomatid flagellates includes several well-studied medically and economically important parasites of vertebrates and plants. Nevertheless, the vast majority of trypanosomatids infect only insects (mostly flies and true bugs) and, because of that, has attracted little research attention in the past. Of several hundred trypanosomatid species, only four can infect bees (honeybees and bumblebees). Because of such scarcity, these parasites are severely understudied. We analyzed whole-genome information for a total of 42 representatives of bee-infecting trypanosomatids collected in Central Europe and Alaska from a population genetics point of view. Our data shed light on the evolution, selection, and diversification in this important group of trypanosomatid parasites.
Faculty of Biology M 5 Lomonosov Moscow State University Moscow Russia
Genetic Diversity Centre ETH Zürich Zürich Switzerland
Institute of Integrative Biology ETH Zürich Zürich Switzerland
Life Science Research Centre Faculty of Science University of Ostrava Ostrava Czech Republic
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Maslov DA, Votýpka J, Yurchenko V, Lukeš J. 2013. Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29:43–52. doi:10.1016/j.pt.2012.11.001. PubMed DOI
Podlipaev SA. 2000. Insect trypanosomatids: the need to know more. Mem Inst Oswaldo Cruz 95:517–522. doi:10.1590/s0074-02762000000400013. PubMed DOI
Kostygov AY, Butenko A, Yurchenko V. 2019. On monoxenous trypanosomatids from lesions of immunocompetent patients with suspected cutaneous leishmaniasis in Iran. Trop Med Int Health 24:127–128. doi:10.1111/tmi.13168. PubMed DOI
Pacheco RS, Marzochi MC, Pires MQ, Brito CM, Madeira MD, Barbosa-Santos EG. 1998. Parasite genotypically related to a monoxenous trypanosomatid of dog’s flea causing opportunistic infection in an HIV positive patient. Mem Inst Oswaldo Cruz 93:531–537. doi:10.1590/S0074-02761998000400021. PubMed DOI
Chicharro C, Alvar J. 2003. Lower trypanosomatids in HIV/AIDS patients. Ann Trop Med Parasitol 97(Suppl 1):75–78. doi:10.1179/000349803225002552. PubMed DOI
Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V. 2018. Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol 34:466–480. doi:10.1016/j.pt.2018.03.002. PubMed DOI
Lukeš J, Skalický T, Týč J, Votýpka J, Yurchenko V. 2014. Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasitol 195:115–122. doi:10.1016/j.molbiopara.2014.05.007. PubMed DOI
Kostygov AY, Yurchenko V. 2017. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia PARASIT 64:20. doi:10.14411/fp.2017.020. PubMed DOI
Schwarz RS, Bauchan GR, Murphy CA, Ravoet J, de Graaf DC, Evans JD. 2015. Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim n. gen., n. sp. J Eukaryot Microbiol 62:567–583. doi:10.1111/jeu.12209. PubMed DOI
Ravoet J, Schwarz RS, Descamps T, Yanez O, Tozkar CO, Martin-Hernandez R, Bartolome C, De Smet L, Higes M, Wenseleers T, Schmid-Hempel R, Neumann P, Kadowaki T, Evans JD, de Graaf DC. 2015. Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim. J Invertebr Pathol 130:21–27. doi:10.1016/j.jip.2015.06.007. PubMed DOI
Schmid-Hempel R, Tognazzo M. 2010. Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. J Eukaryot Microbiol 57:337–345. doi:10.1111/j.1550-7408.2010.00480.x. PubMed DOI
Graystock P, Goulson D, Hughes WO. 2014. The relationship between managed bees and the prevalence of parasites in bumblebees. PeerJ 2:e522. doi:10.7717/peerj.522. PubMed DOI PMC
Durrer S, Schmid-Hempel P. 1994. Shared use of flowers leads to horizontal pathogen transmission. Proc R Soc Lond 258:299–302.
Brown MJF, Schmid-Hempel R, Schmid-Hempel P. 2003. Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. J Anim Ecol 72:994–1002. doi:10.1046/j.1365-2656.2003.00770.x. DOI
Otterstatter MC, Thomson JD. 2008. Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS One 3:e2771. doi:10.1371/journal.pone.0002771. PubMed DOI PMC
Schmid-Hempel R, Eckhardt M, Goulson D, Heinzmann D, Lange C, Plischuk S, Escudero LR, Salathe R, Scriven JJ, Schmid-Hempel P. 2014. The invasion of southern South America by imported bumblebees and associated parasites. J Anim Ecol 83:823–837. doi:10.1111/1365-2656.12185. PubMed DOI
Whitehorn PR, Tinsley MC, Brown MJ, Darvill B, Goulson D. 2011. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proc R Soc B 278:1195–1202. doi:10.1098/rspb.2010.1550. PubMed DOI PMC
Schmid-Hempel P, Puhr K, Kruger N, Reber C, Schmid-Hempel R. 1999. Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53:426–434. doi:10.1111/j.1558-5646.1999.tb03778.x. PubMed DOI
Baer B, Schmid-Hempel P. 2003. Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecol Lett 6:106–110. doi:10.1046/j.1461-0248.2003.00411.x. DOI
Barribeau SM, Schmid-Hempel P. 2013. Qualitatively different immune response of the bumblebee host, Bombus terrestris, to infection by different genotypes of the trypanosome gut parasite, Crithidia bombi. Infect Genet Evol 20:249–256. doi:10.1016/j.meegid.2013.09.014. PubMed DOI
Brunner FS, Schmid-Hempel P, Barribeau SM. 2013. Immune gene expression in Bombus terrestris: signatures of infection despite strong variation among populations, colonies, and sister workers. PLoS One 8:e68181. doi:10.1371/journal.pone.0068181. PubMed DOI PMC
Barribeau SM, Sadd BM, Du Plessis L, Schmid-Hempel P. 2014. Gene expression differences underlying genotype-by-genotype specificity in a host-parasite system. Proc Natl Acad Sci U S A 111:3496–3501. doi:10.1073/pnas.1318628111. PubMed DOI PMC
Schmid-Hempel R, Salathe R, Tognazzo M, Schmid-Hempel P. 2011. Genetic exchange and emergence of novel strains in directly transmitted trypanosomatids. Infect Genet Evol 11:564–571. doi:10.1016/j.meegid.2011.01.002. PubMed DOI
Tognazzo M, Schmid-Hempel R, Schmid-Hempel P. 2012. Probing mixed-genotype infections II: high multiplicity in natural infections of the trypanosomatid, Crithidia bombi, in its host, Bombus spp. PLoS One 7:e49137. doi:10.1371/journal.pone.0049137. PubMed DOI PMC
Wilfert L, Gadau J, Baer B, Schmid-Hempel P. 2007. Natural variation in the genetic architecture of a host-parasite interaction in the bumblebee Bombus terrestris. Mol Ecol 16:1327–1339. doi:10.1111/j.1365-294X.2007.03234.x. PubMed DOI
Ulrich Y, Schmid-Hempel P. 2012. Host modulation of parasite competition in multiple infections. Proc Biol Sci 279:2982–2989. doi:10.1098/rspb.2012.0474. PubMed DOI PMC
Ulrich Y, Sadd BM, Schmid-Hempel P. 2011. Strain filtering and transmission of a mixed infection in a social insect. J Evol Biol 24:354–362. doi:10.1111/j.1420-9101.2010.02172.x. PubMed DOI
Salathé RM, Schmid-Hempel P. 2011. The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap. PLoS One 6:e22054. doi:10.1371/journal.pone.0022054. PubMed DOI PMC
Ruiz-Gonzalez MX, Bryden J, Moret Y, Reber-Funk C, Schmid-Hempel P, Brown MJ. 2012. Dynamic transmission, host quality, and population structure in a multihost parasite of bumblebees. Evolution 66:3053–3066. doi:10.1111/j.1558-5646.2012.01655.x. PubMed DOI
Schmid-Hempel P, Aebi M, Barribeau S, Kitajima T, Du Plessis L, Schmid-Hempel R, Zoller S. 2018. The genomes of Crithidia bombi and C. expoeki, common parasites of bumblebees. PLoS One 13:e0189738. doi:10.1371/journal.pone.0189738. PubMed DOI PMC
Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V. 2019. Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology 146:1–27. doi:10.1017/S0031182018000951. PubMed DOI
Koch H, Woodward J, Langat MK, Brown MJ, Stevenson PC. Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite. Curr Biol, in press. PubMed
Baer B, Schmid-Hempel P. 2001. Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643. doi:10.1111/j.0014-3820.2001.tb00683.x. PubMed DOI
Baer B, Schmid-Hempel P. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154. doi:10.1038/16451. DOI
Schmid-Hempel P. 2001. On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158. doi:10.1007/s001140100222. PubMed DOI
Flegontov P, Butenko A, Firsov S, Kraeva N, Eliáš M, Field MC, Filatov D, Flegontova O, Gerasimov ES, Hlaváčová J, Ishemgulova A, Jackson AP, Kelly S, Kostygov A, Logacheva MD, Maslov DA, Opperdoes FR, O’Reilly A, Sádlová J, Ševčíková T, Venkatesh D, Vlček Č, Volf P, Votýpka J, Záhonová K, Yurchenko V, Lukeš J. 2016. Genome of Leptomonas pyrrhocoris: a high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania. Sci Rep 6:23704. doi:10.1038/srep23704. PubMed DOI PMC
Weir W, Capewell P, Foth B, Clucas C, Pountain A, Steketee P, Veitch N, Koffi M, De Meeus T, Kabore J, Camara M, Cooper A, Tait A, Jamonneau V, Bucheton B, Berriman M, MacLeod A. 2016. Population genomics reveals the origin and asexual evolution of human infective trypanosomes. Elife 5:e11473. doi:10.7554/eLife.11473. PubMed DOI PMC
Bussotti G, Gouzelou E, Côrtes Boité M, Kherachi I, Harrat Z, Eddaikra N, Mottram JC, Antoniou M, Christodoulou V, Bali A, Guerfali FZ, Laouini D, Mukhtar M, Dumetz F, Dujardin J-C, Smirlis D, Lechat P, Pescher P, El Hamouchi A, Lemrani M, Chicharro C, Llanes-Acevedo IP, Botana L, Cruz I, Moreno J, Jeddi F, Aoun K, Bouratbine A, Cupolillo E, Späth GF. 2018. Leishmania genome dynamics during environmental adaptation reveal strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification. mBio 9. doi:10.1128/mBio.01399-18. PubMed DOI PMC
Reis-Cunha JL, Valdivia HO, Bartholomeu DC. 2018. Gene and chromosomal copy number variations as an adaptive mechanism towards a parasitic lifestyle in trypanosomatids. Curr Genomics 19:87–97. PubMed PMC
Yourth CP, Schmid-Hempel P. 2006. Serial passage of the parasite Crithidia bombi within a colony of its host, Bombus terrestris, reduces success in unrelated hosts. Proc R Soc B 273:655–659. doi:10.1098/rspb.2005.3371. PubMed DOI PMC
Tibayrenc M, Ayala FJ. 2013. How clonal are Trypanosoma and Leishmania? Trends Parasitol 29:264–269. doi:10.1016/j.pt.2013.03.007. PubMed DOI
Koffi M, De Meeus T, Sere M, Bucheton B, Simo G, Njiokou F, Salim B, Kabore J, MacLeod A, Camara M, Solano P, Belem AM, Jamonneau V. 2015. Population genetics and reproductive strategies of African trypanosomes: revisiting available published data. PLoS Negl Trop Dis 9:e0003985. doi:10.1371/journal.pntd.0003985. PubMed DOI PMC
Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJ. 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366. doi:10.1038/nature12977. PubMed DOI PMC
Kraeva N, Butenko A, Hlaváčová J, Kostygov A, Myškova J, Grybchuk D, Leštinová T, Votýpka J, Volf P, Opperdoes F, Flegontov P, Lukeš J, Yurchenko V. 2015. Leptomonas seymouri: adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and coinfection with Leishmania donovani. PLoS Pathog 11:e1005127. doi:10.1371/journal.ppat.1005127. PubMed DOI PMC
Votýpka J, Suková E, Kraeva N, Ishemgulova A, Duží I, Lukeš J, Yurchenko V. 2013. Diversity of trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. n. Protist 164:763–781. doi:10.1016/j.protis.2013.08.002. PubMed DOI
Grybchuk-Ieremenko A, Losev A, Kostygov AY, Lukeš J, Yurchenko V. 2014. High prevalence of trypanosome coinfections in freshwater fishes. Folia Parasitol 61:495–504. doi:10.14411/fp.2014.064. PubMed DOI
Hines HM. 2008. Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Syst Biol 57:58–75. doi:10.1080/10635150801898912. PubMed DOI
Freel KC, Friedrich A, Hou J, Schacherer J. 2014. Population genomic analysis reveals highly conserved mitochondrial genomes in the yeast species Lachancea thermotolerans. Genome Biol Evol 6:2586–2594. doi:10.1093/gbe/evu203. PubMed DOI PMC
Ruan J, Cheng J, Zhang T, Jiang H. 2017. Mitochondrial genome evolution in the Saccharomyces sensu stricto complex. PLoS One 12:e0183035. doi:10.1371/journal.pone.0183035. PubMed DOI PMC
Salathé R, Tognazzo M, Schmid-Hempel R, Schmid-Hempel P. 2012. Probing mixed-genotype infections. I. Extraction and cloning of infections from hosts of the trypanosomatid Crithidia bombi. PLoS One 7:e49046. doi:10.1371/journal.pone.0049046. PubMed DOI PMC
Schmid-Hempel P, Schmid-Hempel R. 1993. Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behav Ecol Sociobiol 33:319–327. doi:10.1007/BF00172930. DOI
Votýpka J, d’Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V. 2015. New approaches to systematics of Trypanosomatidae: criteria for taxonomic (re)description. Trends Parasitol 31:460–469. doi:10.1016/j.pt.2015.06.015. PubMed DOI
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi:10.1093/bioinformatics/btu170. PubMed DOI PMC
Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data, http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. doi:10.1038/nmeth.1923. PubMed DOI PMC
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Study. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. doi:10.1093/bioinformatics/btp352. PubMed DOI PMC
Ramirez-Gonzalez RH, Bonnal R, Caccamo M, Maclean D. 2012. Bio-SAMtools: ruby bindings for SAMtools, a library for accessing BAM files containing high-throughput sequence alignments. Source Code Biol Med 7:6. doi:10.1186/1751-0473-7-6. PubMed DOI PMC
Quinlan AR. 2014. BEDTools: the Swiss-Army tool for genome feature analysis. Curr Protoc Bioinformatics 47:11.12.1–11.12.34. doi:10.1002/0471250953.bi1112s47. PubMed DOI PMC
Peterlongo P, Riou C, Drezen E, Lemaitre C. 2017. DiscoSnp++: de novo detection of small variants from raw unassembled read set(s). bioRxiv doi:10.1101/209965. DOI
Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. 2017. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27:722–736. doi:10.1101/gr.215087.116. PubMed DOI PMC
Klambauer G, Schwarzbauer K, Mayr A, Clevert DA, Mitterecker A, Bodenhofer U, Hochreiter S. 2012. cn.MOPS: mixture of Poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res 40:e69. doi:10.1093/nar/gks003. PubMed DOI PMC
Opperdoes FR, Butenko A, Flegontov P, Yurchenko V, Lukeš J. 2016. Comparative metabolism of free-living Bodo saltans and parasitic trypanosomatids. J Eukaryot Microbiol 63:657–678. doi:10.1111/jeu.12315. PubMed DOI
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010. PubMed DOI PMC
Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. doi:10.1093/oxfordjournals.molbev.a026334. PubMed DOI
Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. doi:10.1080/10635150701472164. PubMed DOI
Huerta-Cepas J, Serra F, Bork P. 2016. ETE3: reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 33:1635–1638. doi:10.1093/molbev/msw046. PubMed DOI PMC
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010. PubMed DOI
Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi:10.1093/bioinformatics/btu033. PubMed DOI PMC
Gascuel O. 1997. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695. doi:10.1093/oxfordjournals.molbev.a025808. PubMed DOI
Price MN, Dehal PS, Arkin AP. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650. doi:10.1093/molbev/msp077. PubMed DOI PMC
Alexa A, Rahnenfuhrer J, Lengauer T. 2006. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600–1607. doi:10.1093/bioinformatics/btl140. PubMed DOI
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