- -

Evidence of the Red-Queen hypothesis from accelerated rates of evolution of genes involved in biotic interactions in Pneumocystis

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Evidence of the Red-Queen hypothesis from accelerated rates of evolution of genes involved in biotic interactions in Pneumocystis

Mostrar el registro sencillo del ítem

Ficheros en el ítem

dc.contributor.author Delaye, Luis es_ES
dc.contributor.author Ruiz Ruiz, Susana es_ES
dc.contributor.author Calderon, Enrique es_ES
dc.contributor.author Tarazona Campos, Sonia es_ES
dc.contributor.author Conesa, A. es_ES
dc.contributor.author Moya, Andrés es_ES
dc.date.accessioned 2020-05-22T03:02:52Z
dc.date.available 2020-05-22T03:02:52Z
dc.date.issued 2018-06 es_ES
dc.identifier.issn 1759-6653 es_ES
dc.identifier.uri http://hdl.handle.net/10251/144097
dc.description.abstract [EN] Pneumocystis species are ascomycete fungi adapted to live inside the lungs of mammals. These ascomycetes show extensive stenoxenism, meaning that each species of Pneumocystis infects a single species of host. Here, we study the effect exerted by natural selection on gene evolution in the genomes of three Pneumocystis species. We show that genes involved in host interaction evolve under positive selection. In the first place, we found strong evidence of episodic diversifying selection in Major surface glycoproteins (Msg). These proteins are located on the surface of Pneumocystis and are used for host attachment and probably for immune system evasion. Consistent with their function as antigens, most sites under diversifying selection in Msg code for residues with large relative surface accessibility areas. We also found evidence of positive selection in part of the cell machinery used to export Msg to the cell surface. Specifically, we found that genes participating in glycosylphosphatidylinositol (GPI) biosynthesis show an increased rate of nonsynonymous substitutions (dN) versus synonymous substitutions (dS). GPI is a molecule synthesized in the endoplasmic reticulum that is used to anchor proteins to membranes. We interpret the aforementioned findings as evidence of selective pressure exerted by the host immune system on Pneumocystis species, shaping the evolution of Msg and several proteins involved in GPI biosynthesis. We suggest that genome evolution in Pneumocystis is well described by the Red-Queen hypothesis whereby genes relevant for biotic interactions show accelerated rates of evolution. es_ES
dc.description.sponsorship L.D. wishes to thank Eugenia Flores and Ana Fayos for support provided. This project has received funding from the Marie Curie International Research Staff Exchange Scheme within the 7th European Community Framework Program under grant agreement No 612583-DEANN. Part of this work was done during an internship of L.D. as invited professor at the Universidad de Valencia. Support from CONACYT (grant 454938) is gratefully acknowledged. This work was supported by grants to A.M. from the Spanish Ministry of Science and Competitivity (projects SAF 2012-31187, SAF2013-49788-EXP, SAF2015-65878-R), Carlos III Institute of Health (projects PIE14/00045, AC 15/00022 and AC15/00042), Generalitat Valenciana (project PrometeoII/2014/065) and cofinanced by FEDER. es_ES
dc.language Inglés es_ES
dc.publisher Oxford University Press es_ES
dc.relation.ispartof Genome Biology and Evolution es_ES
dc.rights Reconocimiento - No comercial (by-nc) es_ES
dc.subject Stenoxenism es_ES
dc.subject Majors surface glycoproteins es_ES
dc.subject Glycosylphosphatidylinositol es_ES
dc.subject Natural selection es_ES
dc.subject.classification ESTADISTICA E INVESTIGACION OPERATIVA es_ES
dc.subject.classification BIOQUIMICA Y BIOLOGIA MOLECULAR es_ES
dc.title Evidence of the Red-Queen hypothesis from accelerated rates of evolution of genes involved in biotic interactions in Pneumocystis es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1093/gbe/evy116 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/612583/EU/Developing an European American NGS Network/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//SAF2012-31187/ES/INTERACCION DEL MICROBIOMA Y EL VIROMA DEL INTESTINO HUMANO EN CONDICIONES DE SALUD, ENFERMEDAD Y ESTRES ANTIBIOTICO/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/CONACyT//454938/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//PIE14%2F00045/ES/Identification of novel modulators of chronic inflammation in prevalent diseases: unveiling divergent mechanisms of disease/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/ISCIII//AC 15%2F00022/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//AC15%2F00042/ES/Recognition of the primary infection by Pneumocystis in infants: a silent threat to public health/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEOII%2F2014%2F065/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//SAF2013-49788-EXP/ES/INNOVACION EN MODELOS COMPUTACIONALES PREDICTIVOS EN EPIDEMIOLOGIA EXPERIMENTAL DE LA RESISTENCIA A LOS ANTIBIOTICOS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//SAF2015-65878-R/ES/ESTABILIDAD, RESILIENCIA Y REDUNDANCIA FUNCIONAL DE LA MICROBIOTA INTESTINAL HUMANA DURANTE EL DESARROLLO Y EN RESPUESTA AL ESTRES ANTIBIOTICO Y A CLOSTRIDIUM DIFFICILE/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Estadística e Investigación Operativa Aplicadas y Calidad - Departament d'Estadística i Investigació Operativa Aplicades i Qualitat es_ES
dc.description.bibliographicCitation Delaye, L.; Ruiz Ruiz, S.; Calderon, E.; Tarazona Campos, S.; Conesa, A.; Moya, A. (2018). Evidence of the Red-Queen hypothesis from accelerated rates of evolution of genes involved in biotic interactions in Pneumocystis. Genome Biology and Evolution. 10(6):1596-1606. https://doi.org/10.1093/gbe/evy116 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1093/gbe/evy116 es_ES
dc.description.upvformatpinicio 1596 es_ES
dc.description.upvformatpfin 1606 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 10 es_ES
dc.description.issue 6 es_ES
dc.identifier.pmid 29893833 es_ES
dc.identifier.pmcid PMC6012782 es_ES
dc.relation.pasarela S\366120 es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.contributor.funder Consejo Nacional de Ciencia y Tecnología, México es_ES
dc.description.references Aliouat-Denis, C.-M., Chabé, M., Demanche, C., Aliouat, E. M., Viscogliosi, E., Guillot, J., … Dei-Cas, E. (2008). Pneumocystis species, co-evolution and pathogenic power. Infection, Genetics and Evolution, 8(5), 708-726. doi:10.1016/j.meegid.2008.05.001 es_ES
dc.description.references Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., … Sherlock, G. (2000). Gene Ontology: tool for the unification of biology. Nature Genetics, 25(1), 25-29. doi:10.1038/75556 es_ES
dc.description.references Brockhurst, M. A., Chapman, T., King, K. C., Mank, J. E., Paterson, S., & Hurst, G. D. D. (2014). Running with the Red Queen: the role of biotic conflicts in evolution. Proceedings of the Royal Society B: Biological Sciences, 281(1797), 20141382. doi:10.1098/rspb.2014.1382 es_ES
dc.description.references Brown, G. D., Denning, D. W., Gow, N. A. R., Levitz, S. M., Netea, M. G., & White, T. C. (2012). Hidden Killers: Human Fungal Infections. Science Translational Medicine, 4(165), 165rv13-165rv13. doi:10.1126/scitranslmed.3004404 es_ES
dc.description.references Cagan, A., Theunert, C., Laayouni, H., Santpere, G., Pybus, M., Casals, F., … Andrés, A. M. (2016). Natural Selection in the Great Apes. Molecular Biology and Evolution, 33(12), 3268-3283. doi:10.1093/molbev/msw215 es_ES
dc.description.references Catherinot, E., Lanternier, F., Bougnoux, M.-E., Lecuit, M., Couderc, L.-J., & Lortholary, O. (2010). Pneumocystis jirovecii Pneumonia. Infectious Disease Clinics of North America, 24(1), 107-138. doi:10.1016/j.idc.2009.10.010 es_ES
dc.description.references Chagas, C. (1909). Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Memórias do Instituto Oswaldo Cruz, 1(2), 159-218. doi:10.1590/s0074-02761909000200008 es_ES
dc.description.references Cissé, O. H., Pagni, M., & Hauser, P. M. (2014). Comparative Genomics Suggests That the Human Pathogenic Fungus Pneumocystis jirovecii Acquired Obligate Biotrophy through Gene Loss. Genome Biology and Evolution, 6(8), 1938-1948. doi:10.1093/gbe/evu155 es_ES
dc.description.references Cushion, M. T., Smulian, A. G., Slaven, B. E., Sesterhenn, T., Arnold, J., Staben, C., … Meller, J. (2007). Transcriptome of Pneumocystis carinii during Fulminate Infection: Carbohydrate Metabolism and the Concept of a Compatible Parasite. PLoS ONE, 2(5), e423. doi:10.1371/journal.pone.0000423 es_ES
dc.description.references Daub, J. T., Moretti, S., Davydov, I. I., Excoffier, L., & Robinson-Rechavi, M. (2017). Detection of Pathways Affected by Positive Selection in Primate Lineages Ancestral to Humans. Molecular Biology and Evolution, 34(6), 1391-1402. doi:10.1093/molbev/msx083 es_ES
dc.description.references Deitsch, K. W., Lukehart, S. A., & Stringer, J. R. (2009). Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nature Reviews Microbiology, 7(7), 493-503. doi:10.1038/nrmicro2145 es_ES
dc.description.references Demanche, C., Berthelemy, M., Petit, T., Polack, B., Wakefield, A. E., Dei-Cas, E., & Guillot, J. (2001). Phylogeny of Pneumocystis carinii from 18 Primate Species Confirms Host Specificity and Suggests Coevolution. Journal of Clinical Microbiology, 39(6), 2126-2133. doi:10.1128/jcm.39.6.2126-2133.2001 es_ES
dc.description.references Derouiche, S., Deville, M., Taylor, M., Akbar, H., Guillot, J., Carreto-Binaghi, L., … Demanche, C. (2009). Pneumocystis diversity as a phylogeographic tool. Memórias do Instituto Oswaldo Cruz, 104(1), 112-117. doi:10.1590/s0074-02762009000100017 es_ES
dc.description.references Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792-1797. doi:10.1093/nar/gkh340 es_ES
dc.description.references Edman, J. C., Kovacs, J. A., Masur, H., Santi, D. V., Elwood, H. J., & Sogin, M. L. (1988). Ribosomal RNA sequence shows Pneumocystis carinii to be a member of the Fungi. Nature, 334(6182), 519-522. doi:10.1038/334519a0 es_ES
dc.description.references Finn, R. D., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Mistry, J., Mitchell, A. L., … Bateman, A. (2015). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research, 44(D1), D279-D285. doi:10.1093/nar/gkv1344 es_ES
dc.description.references Fujita, M., & Kinoshita, T. (2009). Structural remodeling of GPI anchors during biosynthesis and after attachment to proteins. FEBS Letters, 584(9), 1670-1677. doi:10.1016/j.febslet.2009.10.079 es_ES
dc.description.references Gerton, J. L., DeRisi, J., Shroff, R., Lichten, M., Brown, P. O., & Petes, T. D. (2000). Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, 97(21), 11383-11390. doi:10.1073/pnas.97.21.11383 es_ES
dc.description.references Gotz, S., Garcia-Gomez, J. M., Terol, J., Williams, T. D., Nagaraj, S. H., Nueda, M. J., … Conesa, A. (2008). High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research, 36(10), 3420-3435. doi:10.1093/nar/gkn176 es_ES
dc.description.references Guindon, S., Dufayard, J.-F., 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. Systematic Biology, 59(3), 307-321. doi:10.1093/sysbio/syq010 es_ES
dc.description.references Hall, J. P. J., Wang, H., & Barry, J. D. (2013). Mosaic VSGs and the Scale of Trypanosoma brucei Antigenic Variation. PLoS Pathogens, 9(7), e1003502. doi:10.1371/journal.ppat.1003502 es_ES
dc.description.references Hauser, P. M. (2014). Genomic Insights into the Fungal Pathogens of the Genus Pneumocystis: Obligate Biotrophs of Humans and Other Mammals. PLoS Pathogens, 10(11), e1004425. doi:10.1371/journal.ppat.1004425 es_ES
dc.description.references Huerta-Cepas, J., Serra, F., & Bork, P. (2016). ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data. Molecular Biology and Evolution, 33(6), 1635-1638. doi:10.1093/molbev/msw046 es_ES
dc.description.references Hughes, A. L. (2007). Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity, 99(4), 364-373. doi:10.1038/sj.hdy.6801031 es_ES
dc.description.references Jackson, A. P., Otto, T. D., Darby, A., Ramaprasad, A., Xia, D., Echaide, I. E., … Pain, A. (2014). The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction. Nucleic Acids Research, 42(11), 7113-7131. doi:10.1093/nar/gku322 es_ES
dc.description.references Keely, S. P., Renauld, H., Wakefield, A. E., Cushion, M. T., Smulian, A. G., Fosker, N., … Hall, N. (2005). Gene Arrays atPneumocystis cariniiTelomeres. Genetics, 170(4), 1589-1600. doi:10.1534/genetics.105.040733 es_ES
dc.description.references Keely, S. P., & Stringer, J. R. (2009). Complexity of the MSG gene family of Pneumocystis carinii. BMC Genomics, 10(1), 367. doi:10.1186/1471-2164-10-367 es_ES
dc.description.references Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H., & Frost, S. D. W. (2006). GARD: a genetic algorithm for recombination detection. Bioinformatics, 22(24), 3096-3098. doi:10.1093/bioinformatics/btl474 es_ES
dc.description.references Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33(7), 1870-1874. doi:10.1093/molbev/msw054 es_ES
dc.description.references Kutty, G., England, K. J., & Kovacs, J. A. (2013). Expression of Pneumocystis jirovecii Major Surface Glycoprotein in Saccharomyces cerevisiae. The Journal of Infectious Diseases, 208(1), 170-179. doi:10.1093/infdis/jit131 es_ES
dc.description.references Kutty, G., Maldarelli, F., Achaz, G., & Kovacs, J. A. (2008). Variation in the Major Surface Glycoprotein Genes inPneumocystis jirovecii. The Journal of Infectious Diseases, 198(5), 741-749. doi:10.1086/590433 es_ES
dc.description.references Kutty, G., Shroff, R., & Kovacs, J. A. (2013). Characterization of Pneumocystis Major Surface Glycoprotein Gene (msg) Promoter Activity in Saccharomyces cerevisiae. Eukaryotic Cell, 12(10), 1349-1355. doi:10.1128/ec.00122-13 es_ES
dc.description.references Kyes, S. A., Kraemer, S. M., & Smith, J. D. (2007). Antigenic Variation in Plasmodium falciparum: Gene Organization and Regulation of the var Multigene Family. Eukaryotic Cell, 6(9), 1511-1520. doi:10.1128/ec.00173-07 es_ES
dc.description.references Li, L. (2003). OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes. Genome Research, 13(9), 2178-2189. doi:10.1101/gr.1224503 es_ES
dc.description.references Liang, M., Raley, C., Zheng, X., Kutty, G., Gogineni, E., Sherman, B. T., … Huang, D. W. (2016). Distinguishing highly similar gene isoforms with a clustering-based bioinformatics analysis of PacBio single-molecule long reads. BioData Mining, 9(1). doi:10.1186/s13040-016-0090-8 es_ES
dc.description.references Ma, L., Chen, Z., Huang, D. W., Kutty, G., Ishihara, M., Wang, H., … Kovacs, J. A. (2016). Genome analysis of three Pneumocystis species reveals adaptation mechanisms to life exclusively in mammalian hosts. Nature Communications, 7(1). doi:10.1038/ncomms10740 es_ES
dc.description.references Mancera, E., Bourgon, R., Brozzi, A., Huber, W., & Steinmetz, L. M. (2008). High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature, 454(7203), 479-485. doi:10.1038/nature07135 es_ES
dc.description.references Murrell, B., Wertheim, J. O., Moola, S., Weighill, T., Scheffler, K., & Kosakovsky Pond, S. L. (2012). Detecting Individual Sites Subject to Episodic Diversifying Selection. PLoS Genetics, 8(7), e1002764. doi:10.1371/journal.pgen.1002764 es_ES
dc.description.references Palmer, G. H., & Brayton, K. A. (2007). Gene conversion is a convergent strategy for pathogen antigenic variation. Trends in Parasitology, 23(9), 408-413. doi:10.1016/j.pt.2007.07.008 es_ES
dc.description.references Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics, 20(2), 289-290. doi:10.1093/bioinformatics/btg412 es_ES
dc.description.references Paterson, S., Vogwill, T., Buckling, A., Benmayor, R., Spiers, A. J., Thomson, N. R., … Brockhurst, M. A. (2010). Antagonistic coevolution accelerates molecular evolution. Nature, 464(7286), 275-278. doi:10.1038/nature08798 es_ES
dc.description.references Petersen, B., Petersen, T., Andersen, P., Nielsen, M., & Lundegaard, C. (2009). A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Structural Biology, 9(1), 51. doi:10.1186/1472-6807-9-51 es_ES
dc.description.references Petes, T. D. (2001). Meiotic recombination hot spots and cold spots. Nature Reviews Genetics, 2(5), 360-369. doi:10.1038/35072078 es_ES
dc.description.references Pittet, M., & Conzelmann, A. (2007). Biosynthesis and function of GPI proteins in the yeast Saccharomyces cerevisiae. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1771(3), 405-420. doi:10.1016/j.bbalip.2006.05.015 es_ES
dc.description.references Pond, S. L. K., Frost, S. D. W., & Muse, S. V. (2004). HyPhy: hypothesis testing using phylogenies. Bioinformatics, 21(5), 676-679. doi:10.1093/bioinformatics/bti079 es_ES
dc.description.references Schmid-Siegert, E., Richard, S., Luraschi, A., Mühlethaler, K., Pagni, M., & Hauser, P. M. (2017). Mechanisms of Surface Antigenic Variation in the Human Pathogenic Fungus Pneumocystis jirovecii. mBio, 8(6). doi:10.1128/mbio.01470-17 es_ES
dc.description.references Serra, F., Arbiza, L., Dopazo, J., & Dopazo, H. (2011). Natural Selection on Functional Modules, a Genome-Wide Analysis. PLoS Computational Biology, 7(3), e1001093. doi:10.1371/journal.pcbi.1001093 es_ES
dc.description.references STRINGER, J. R. (2007). Antigenic Variation in Pneumocystis. The Journal of Eukaryotic Microbiology, 54(1), 8-13. doi:10.1111/j.1550-7408.2006.00225.x es_ES
dc.description.references Stringer, S. L., Stringer, J. R., Blase, M. A., Walzer, P. D., & Cushion, M. T. (1989). Pneumocystis carinii: Sequence from ribosomal RNA implies a close relationship with fungi. Experimental Parasitology, 68(4), 450-461. doi:10.1016/0014-4894(89)90130-6 es_ES
dc.description.references Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., … Mesirov, J. P. (2005). Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences, 102(43), 15545-15550. doi:10.1073/pnas.0506580102 es_ES
dc.description.references Thomas, C. F., & Limper, A. H. (2007). Current insights into the biology and pathogenesis of Pneumocystis pneumonia. Nature Reviews Microbiology, 5(4), 298-308. doi:10.1038/nrmicro1621 es_ES
dc.description.references Vink, C., Rudenko, G., & Seifert, H. S. (2012). Microbial antigenic variation mediated by homologous DNA recombination. FEMS Microbiology Reviews, 36(5), 917-948. doi:10.1111/j.1574-6976.2011.00321.x es_ES
dc.description.references Vinuesa, P., & Contreras-Moreira, B. (2015). Robust Identification of Orthologues and Paralogues for Microbial Pan-Genomics Using GET_HOMOLOGUES: A Case Study of pIncA/C Plasmids. Bacterial Pangenomics, 203-232. doi:10.1007/978-1-4939-1720-4_14 es_ES
dc.description.references Weatherly, D. B., Peng, D., & Tarleton, R. L. (2016). Recombination-driven generation of the largest pathogen repository of antigen variants in the protozoan Trypanosoma cruzi. BMC Genomics, 17(1). doi:10.1186/s12864-016-3037-z es_ES
dc.description.references Yang, Z. (2007). PAML 4: Phylogenetic Analysis by Maximum Likelihood. Molecular Biology and Evolution, 24(8), 1586-1591. doi:10.1093/molbev/msm088 es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem