Highly Resolved Genomes of Two Closely Related Lineages of the Rodent Louse Polyplax serrata with Different Host Specificities
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
21-02532S to V.H
Grant Agency of the Czech Republic
PubMed
38478715
PubMed Central
PMC10972687
DOI
10.1093/gbe/evae045
PII: 7628191
Knihovny.cz E-zdroje
- Klíčová slova
- Anoplura, genomics, sucking lice, symbiosis,
- MeSH
- Anoplura * genetika MeSH
- fylogeneze MeSH
- hlodavci genetika MeSH
- hostitelská specificita genetika MeSH
- Legionella * MeSH
- lidé MeSH
- Pediculus * genetika MeSH
- vitamin B komplex * MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- vitamin B komplex * MeSH
Sucking lice of the parvorder Anoplura are permanent ectoparasites with specific lifestyle and highly derived features. Currently, genomic data are only available for a single species, the human louse Pediculus humanus. Here, we present genomes of two distinct lineages, with different host spectra, of a rodent louse Polyplax serrata. Genomes of these ecologically different lineages are closely similar in gene content and display a conserved order of genes, with the exception of a single translocation. Compared with P. humanus, the P. serrata genomes are noticeably larger (139 vs. 111 Mbp) and encode a higher number of genes. Similar to P. humanus, they are reduced in sensory-related categories such as vision and olfaction. Utilizing genome-wide data, we perform phylogenetic reconstruction and evolutionary dating of the P. serrata lineages. Obtained estimates reveal their relatively deep divergence (∼6.5 Mya), comparable with the split between the human and chimpanzee lice P. humanus and Pediculus schaeffi. This supports the view that the P. serrata lineages are likely to represent two cryptic species with different host spectra. Historical demographies show glaciation-related population size (Ne) reduction, but recent restoration of Ne was seen only in the less host-specific lineage. Together with the louse genomes, we analyze genomes of their bacterial symbiont Legionella polyplacis and evaluate their potential complementarity in synthesis of amino acids and B vitamins. We show that both systems, Polyplax/Legionella and Pediculus/Riesia, display almost identical patterns, with symbionts involved in synthesis of B vitamins but not amino acids.
Zobrazit více v PubMed
Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, Aksoy S. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet. 2002:32(3):402–407. 10.1038/ng986. PubMed DOI
Allen JM, Reed DL, Perotti MA, Braig HR. Evolutionary relationships of “Candidatus Riesia spp.,” endosymbiotic enterobacteriaceae living within hematophagous primate lice. Appl Environ Microbiol. 2007:73(5):1659–1664. 10.1128/AEM.01877-06. PubMed DOI PMC
Almagro Armenteros JJ, Tsirigos KD, Sonderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019:37(4):420–423. 10.1038/s41587-019-0036-z. PubMed DOI
Ammar E, Tsai C, Whitfield A, Redinbaugh M, Hogenhout S. Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Annu Rev Entomol. 2009:54(1):447–468. 10.1146/annurev.ento.54.110807.090454. PubMed DOI
Andrews S. FastQC: a quality control tool for high throughput sequence data. 2010. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Baldwin-Brown J, Villa S, Vickrey A, Johnson K, Bush S, Clayton D, Shapiro M. The assembled and annotated genome of the pigeon louse Columbicola columbae, a model ectoparasite. G3. 2021:11(2):jkab009. 10.1093/g3journal/jkab009. PubMed DOI PMC
Bandi V, Gutwin C. Proceedings of the 46th Graphics Interface Conference on Proceedings of Graphics Interface. Waterloo (ON): Canadian Human-Computer Communications Society; 2020. p. 74–83.
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, et al. . SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012:19(5):455–477. 10.1089/cmb.2012.0021. PubMed DOI PMC
Bolger A, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014:30(15):2114–2120. 10.1093/bioinformatics/btu170. PubMed DOI PMC
Boyd BM, Allen JM, de Crécy-Lagard V, Reed DL. Genome sequence of Candidatus Riesia pediculischaeffi, endosymbiont of chimpanzee lice, and genomic comparison of recently acquired endosymbionts from human and chimpanzee lice. G3. 2014:4(11):2189–2195. 10.1534/g3.114.012567. PubMed DOI PMC
Cantalapiedra C, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol. 2021:38(12):5825–5829. 10.1093/molbev/msab293. PubMed DOI PMC
Danecek P, Bonfield J, Liddle J, Marshall J, Ohan V, Pollard M, Whitwham A, Keane T, McCarthy S, Davies R, et al. . Twelve years of SAMtools and BCFtools. GigaScience 2021:10(2):giab008. 10.1093/gigascience/giab008. PubMed DOI PMC
de Moya R, Yoshizawa K, Walden K, Sweet A, Dietrich C, Johnson KP. Phylogenomics of parasitic and nonparasitic lice (Insecta: Psocodea): combining sequence data and exploring compositional bias solutions in next generation data sets. Syst Biol. 2021:70(4):719–738. 10.1093/sysbio/syaa075. PubMed DOI
Ding Q, Li R, Ren X, Chan L, Ho V, Xie D, Ye P, Zhao Z. Genomic architecture of 5S rDNA cluster and its variations within and between species. BMC Genomics. 2022:23(1):238. 10.1186/s12864-022-08476-x. PubMed DOI PMC
Drula E, Garron ML, Dogan S, Lombard V, Henrissat B, Terrapon N. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. 2022:50(D1):D571–D577. 10.1093/nar/gkab1045. PubMed DOI PMC
Emms D, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015:16(1):157. 10.1186/s13059-015-0721-2. PubMed DOI PMC
Feulner P, De-Kayne R. Genome evolution, structural rearrangements and speciation. J Evol Biol. 2017:30(8):1488–1490. 10.1111/jeb.13101. PubMed DOI
Flynn J, Hubley R, Goubert C, Rosen J, Clark A, Feschotte C, Smit A. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci USA. 2020:117(17):9451–9457. 10.1073/pnas.1921046117. PubMed DOI PMC
Golub N, Nokkala S. Brief report—chromosome numbers of two sucking louse species (Insecta, Phthiraptera, Anoplura). Hereditas 2004:141(1):94–96. 10.1111/j.1601-5223.2004.01859.x. PubMed DOI
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011:29(7):644–652. 10.1038/nbt.1883. PubMed DOI PMC
Hoff KJ, Stanke M. Predicting genes in single genomes with AUGUSTUS. Curr Protoc Bioinformatics. 2019:65(1):e57. 10.1002/cpbi.57. PubMed DOI
Kall L, Krogh A, Sonnhammer EL. A combined transmembrane topology and signal peptide prediction method. J Mol Biol. 2004:338(5):1027–1036. 10.1016/j.jmb.2004.03.016. PubMed DOI
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2016:44(D1):D457–D462. 10.1093/nar/gkv1070. PubMed DOI PMC
Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016:428(4):726–731. 10.1016/j.jmb.2015.11.006. PubMed DOI
Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002:30(14):3059–3066. 10.1093/nar/gkf436. PubMed DOI PMC
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, et al. . Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012:28(12):1647–1649. 10.1093/bioinformatics/bts199. PubMed DOI PMC
Kinjo Y, Bourguignon T, Hongoh Y, Lo N, Tokuda G, Ohkuma M. Coevolution of metabolic pathways in Blattodea and their Blattabacterium endosymbionts, and comparisons with other insect-bacteria symbioses: Microbiology Spectrum. 2022:10:e02779-22. PubMed PMC
Kirkness EF, Haas BJ, Sun WL, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, et al. . Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA. 2010:107(27):12168–12173. 10.1073/pnas.1003379107. PubMed DOI PMC
Kolesov G, Mewes HW, Frishman D. SNAPping up functionally related genes based on context information: a colinearity-free approach. J Mol Biol. 2001:311(4):639–656. 10.1006/jmbi.2001.4701. PubMed DOI
Kolmogorov M, Yuan J, Lin Y, Pevzner P. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019:37(5):540–546. 10.1038/s41587-019-0072-8. PubMed DOI
Langmead B, Salzberg S. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012:9(4):357–359. 10.1038/nmeth.1923. PubMed DOI PMC
Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, Park Y, Buso N, Lopez R. The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res. 2015:43(W1):W580–W584. 10.1093/nar/gkv279. PubMed DOI PMC
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009:25(16):2078–2079. 10.1093/bioinformatics/btp352. PubMed DOI PMC
Light J, Smith V, Allen J, Durden L, Reed D. Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura). BMC Evol Biol. 2010:10(1):292. 10.1186/1471-2148-10-292. PubMed DOI PMC
Longdon B, Day J, Schulz N, Leftwich P, de Jong M, Breuker C, Gibbs M, Obbard D, Wilfert L, Smith S, et al. . Vertically transmitted rhabdoviruses are found across three insect families and have dynamic interactions with their hosts. Proc R Soc B Biol Sci. 2017:284(1847):20162381. 10.1098/rspb.2016.2381. PubMed DOI PMC
Lukashin AV, Borodovsky M. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 1998:26(4):1107–1115. 10.1093/nar/26.4.1107. PubMed DOI PMC
Majoros WH, Pertea M, Salzberg SL. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics. 2004:20(16):2878–2879. 10.1093/bioinformatics/bth315. PubMed DOI
Martinů J, Hypša V, Štefka J. Host specificity driving genetic structure and diversity in ectoparasite populations: coevolutionary patterns in Apodemus mice and their lice. Ecol Evol. 2018:8(20):10008–10022. 10.1002/ece3.4424. PubMed DOI PMC
Martinů J, Roubová V, Nováková M, Smith VS, Hypša V, Stefka J. Characterisation of microsatellite loci in two species of lice, Polyplax serrata (Phthiraptera: Anoplura: Polyplacidae) and Myrsidea nesomimi (Phthiraptera: Amblycera: Menoponidae). Folia Parasitol. 2015:62:16. 10.14411/fp.2015.016. PubMed DOI
Martinů J, Štefka J, Poosakkannu A, Hypša V. “Parasite turnover zone” at secondary contact: a new pattern in host-parasite population genetics. Mol Ecol. 2020:29(23):4653–4664. 10.1111/mec.15653. PubMed DOI
Mendes F, Vanderpool D, Fulton B, Hahn M. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics. 2020:36(22-23):5516–5518. 10.1093/bioinformatics/btaa1022. PubMed DOI
Michaux J, Libois R, Filippucci M. So close and so different: comparative phylogeography of two small mammal species, the yellow-necked fieldmouse (Apodemus flavicollis) and the woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity (Edinb). 2005:94(1):52–63. 10.1038/sj.hdy.6800561. PubMed DOI
Michaux J, Pasquier L. Dynamique des populations de mulots (Rodentia, Apodemus) en Europe durant le Quaternaire; premieres donnees. Bull Soc Géol France. 1974:S7-XVI(4):431–439. 10.2113/gssgfbull.S7-XVI.4.431. DOI
Minh B, Schmidt H, Chernomor O, Schrempf D, Woodhams M, von Haeseler A, Lanfear R. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020:37(8):2461–2461. 10.1093/molbev/msaa131. PubMed DOI PMC
Oksanen J. vegan: an R package for community ecologists. 2022. https://github.com/vegandevs/vegan
Paysan-Lafosse T, Blum M, Chuguransky S, Grego T, Pinto B, Salazar G, Bileschi M, Bork P, Bridge A, Colwell L, et al. . InterPro in 2022. Nucleic Acids Res. 2023:51(D1):D418–D427. 10.1093/nar/gkac993. PubMed DOI PMC
Puttick M. MCMCtreeR: functions to prepare MCMCtree analyses and visualize posterior ages on trees. Bioinformatics. 2019:35(24):5321–5322. 10.1093/bioinformatics/btz554. PubMed DOI
R Core Team R . R: a language and environment for statistical computing.2013. https://www.r-project.org/
Reed D, Light J, Allen J, Kirchman J. Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol. 2007:5(1):7. 10.1186/1741-7007-5-7. PubMed DOI PMC
Říhová JM, Gupta S, Darby AC, Nováková E, Hypša V. Arsenophonus symbiosis with louse flies: multiple origins, coevolutionary dynamics, and metabolic significance. mSystems. 8(5):e0070623. 10.1128/msystems.00706-23. PubMed DOI PMC
Říhová J, Nováková E, Husník F, Hypša V. Legionella becoming a mutualist: adaptive processes shaping the genome of symbiont in the louse Polyplax serrata. Genome Biol Evol. 2017:9(11):2946–2957. 10.1093/gbe/evx217. PubMed DOI PMC
Rio RVM, Symula RE, Wang JW, Lohs C, Wu YN, Snyder AK, Bjornson RD, Oshima K, Biehl BS, Perna NT, et al. . Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: Glossinidae) obligate symbiont Wigglesworthia. mBio. 2012:3(1):e00240-11. 10.1128/mBio.00240-11. PubMed DOI PMC
Romiguier J, Lourenco J, Gayral P, Faivre N, Weinert L, Ravel S, Ballenghien M, Cahais V, Bernard A, Loire E, et al. . Population genomics of eusocial insects: the costs of a vertebrate-like effective population size. J Evol Biol. 2014:27(3):593–603. 10.1111/jeb.12331. PubMed DOI
Salzberg S. Next-generation genome annotation: we still struggle to get it right. Genome Biol. 2019:20(1):92. 10.1186/s13059-019-1715-2. PubMed DOI PMC
Scalzitti N, Jeannin-Girardon A, Collet P, Poch O, Thompson J. A benchmark study of ab initio gene prediction methods in diverse eukaryotic organisms. BMC Genomics. 2020:21(1):293. 10.1186/s12864-020-6707-9. PubMed DOI PMC
Schiffels S, Durbin R. Inferring human population size and separation history from multiple genome sequences. Nat Genet. 2014:46:919–925. 10.1038/ng.3015. PubMed DOI PMC
Schiffels S, Wang K.. MSMC and MSMC2: the Multiple Sequentially Markovian Coalescent. In: Dutheil JY, editor. Statistical population genomics. Methods in Molecular Biology. New York (NY): Humana; 2020. p. 147–1662090. PubMed
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014:30(14):2068–2069. 10.1093/bioinformatics/btu153. PubMed DOI
Shin C, Allmon W. How we study cryptic species and their biological implications: a case study from marine shelled gastropods. Ecol Evol. 2023:13(9):e10360. 10.1002/ece3.10360. PubMed DOI PMC
Simakov O, Marlétaz F, Yue J, O'Connell B, Jenkins J, Brandt A, Calef R, Tung C, Huang T, Schmutz J, et al. . Deeply conserved synteny resolves early events in vertebrate evolution. Nat Ecol Evol. 2020:4(6):820–830. 10.1038/s41559-020-1156-z. PubMed DOI PMC
Štefka J, Hypša V. Host specificity and genealogy of the louse Polyplax serrata on field mice, Apodemus species: a case of parasite duplication or colonisation? Int J Parasitol. 2008:38(6):731–741. 10.1016/j.ijpara.2007.09.011. PubMed DOI
Sun J, Lu F, Luo Y, Bie L, Xu L, Wang Y. OrthoVenn3: an integrated platform for exploring and visualizing orthologous data across genomes. Nucleic Acids Res. 2023:51(W1):W397–W403. 10.1093/nar/gkad313. PubMed DOI PMC
Sweet A, Browne D, Hernandez A, Johnson K, Cameron S. Draft genome assemblies of the avian louse Brueelia nebulosa and its associates using long-read sequencing from an individual specimen. G3. 2023:13(4):jkad030. 10.1093/g3journal/jkad030. PubMed DOI PMC
Tarailo-Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinform 2009:Chapter 4:4.10.1–4.10.14. 10.1002/0471250953.bi0410s25. PubMed DOI
Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, Del Angel G, Levy-Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J, et al. . From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Current Protoc Bioinform. 2013:43(1):11.10.1–11.10.33. 10.1002/0471250953.bi1110s43. PubMed DOI PMC
Wang Y, McNeil P, Abdulazeez R, Pascual M, Johnston S, Keightley P, Obbard D. Variation in mutation, recombination, and transposition rates in Drosophila melanogaster and Drosophila simulans. Genome Res. 2023:33(4):587–598. 10.1101/gr.277383.122. PubMed DOI PMC
Wang Y, Tang H, DeBarry J, Tan X, Li J, Wang X, Lee T, Jin H, Marler B, Guo H, et al. . MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012:40(7):e49. 10.1093/nar/gkr1293. PubMed DOI PMC
Waterhouse R, Seppey M, Simao F, Manni M, Ioannidis P, Klioutchnikov G, Kriventseva E, Zdobnov E. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol. 2018:35(3):543–548. 10.1093/molbev/msx319. PubMed DOI PMC
Xu Z, Mai Y, Liu D, He W, Lin X, Xu C, Zhang L, Meng X, Mafofo J, Zaher WA, et al. . Fast-bonito: a faster deep learning based basecaller for nanopore sequencing. Artif Intell Life Sci. 2021:1:100011. 10.1016/j.ailsci.2021.100011. DOI
Zdobnov EM, Apweiler R. InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics. 2001:17(9):847–848. 10.1093/bioinformatics/17.9.847. PubMed DOI