Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-29T05:07:16.007Z Has data issue: false hasContentIssue false

Genetic diversity and evolution of Pneumocystis fungi infecting wild Southeast Asian murid rodents

Published online by Cambridge University Press:  09 November 2017

Alice Latinne*
Affiliation:
Institut des Sciences de l'Evolution (ISEM), UMR 5554 CNRS-IRD-UM2, CC65, Université de Montpellier 2, Montpellier, France Departement of Life Sciences-Conservation Genetics, University of Liège, Liège, Belgium EcoHealth Alliance, New York, USA
François Bezé
Affiliation:
Medical Laboratory, Dunkerque Hospital, Dunkerque, France Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France
Laurence Delhaes
Affiliation:
Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France Service de Parasitologie-Mycologie – ISERM U1045, CHU de Bordeaux, Université de Bordeaux, France
Muriel Pottier
Affiliation:
Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France
Nausicaa Gantois
Affiliation:
Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France
Julien Nguyen
Affiliation:
Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France
Kim Blasdell
Affiliation:
CSIRO Health and Biosecurity Business Unit, Australian Animal Health Laboratory, Geelong, Australia
Eduardo Dei-Cas
Affiliation:
Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France
Serge Morand
Affiliation:
Institut des Sciences de l'Evolution (ISEM), UMR 5554 CNRS-IRD-UM2, CC65, Université de Montpellier 2, Montpellier, France CNRS-CIRAD, Centre Infectiologie Christophe Mérieux du Laos, Vientiane, LAOS PDR
Magali Chabé
Affiliation:
Univ. Lille, CNRS, Inserm, CHU de Lille, Institut Pasteur de Lille, U1019 – UMR 8204 – CIIL – Center for Infection and Immunity of Lille, Lille, France
*
Author for correspondence: Alice Latinne, E-mail: latinne@ecohealthalliance.org

Abstract

Pneumocystis organisms are airborne-transmitted fungal parasites that infect the lungs of numerous mammalian species with strong host specificity. In this study, we investigated the genetic diversity and host specificity of Pneumocystis organisms infecting Southeast Asian murid rodents through PCR amplification of two mitochondrial genes and tested the co-phylogeny hypothesis among these fungi and their rodent hosts. Pneumocystis DNA was detected in 215 of 445 wild rodents belonging to 18 Southeast Asian murid species. Three of the Pneumocystis lineages retrieved in our phylogenetic trees correspond to known Pneumocystis species, but some of the remaining lineages may correspond to new undescribed species. Most of these Pneumocystis species infect several rodent species or genera and some sequence types are shared among several host species and genera. These results indicated a weaker host specificity of Pneumocystis species infecting rodents than previously thought. Our co-phylogenetic analyses revealed a complex evolutionary history among Pneumocystis and their rodent hosts. Even if a significant global signal of co-speciation has been detected, co-speciation alone is not sufficient to explain the observed co-phylogenetic pattern and several host switches are inferred. These findings conflict with the traditional view of a prolonged process of co-evolution and co-speciation of Pneumocystis and their hosts.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agosta, SJ and Klemens, JA (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecology Letters 11, 11231134.CrossRefGoogle ScholarPubMed
Akbar, H, Pinçon, C, Aliouat-Denis, C-M, Derouiche, S, Taylor, M-L, Pottier, M, Carreto-Binaghi, L-H, González-González, AE, Courpon, A, Barriel, V, Guillot, J, Chabé, M, Suarez-Alvarez, RO, Aliouat, EM, Dei-Cas, E and Demanche, C (2012) Characterizing Pneumocystis in the lungs of bats: understanding Pneumocystis evolution and the spread of Pneumocystis organisms in mammal populations. Applied and Environmental Microbiology 78, 81228136.Google Scholar
Aliouat, EM, Mazars, E, Dei-Cas, E, Cesbron, JY and Camus, D (1993) Intranasal inoculation of mouse, rat or rabbit-derived Pneumocystis to SCID mice. Journal of Protozoology Research 3, 9498.Google Scholar
Aliouat, EM, Mazars, E, Dei-Cas, E, Delcourt, P, Billaut, P and Camus, D (1994) Pneumocystis cross infection experiments using SCID mice and nude rats as recipient host, showed strong host-species specificity. Journal of Eukaryotic Microbiology 41, 71S.Google ScholarPubMed
Aliouat-Denis, CM, Chabé, M, Demanche, C, Aliouat, EM, Viscogliosi, E, Guillot, J, Delhaes, L and Dei-Cas, E (2008) Pneumocystis species, co-evolution and pathogenic power. Infection, Genetics and Evolution 8, 708726.Google Scholar
Aplin, KP, Brown, PR, Jacobs, J, Krebs, CJ and Singleton, GR (2003) Field Methods for Rodent Studies in Asia and the Indo-Pacific. Canberra: ACIAR.Google Scholar
Araujo, SBL, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS ONE 10, e0139225.CrossRefGoogle ScholarPubMed
Balbuena, JA, Míguez-Lozano, R and Blasco-Costa, I (2013) PACo: a novel procrustes application to cophylogenetic analysis. PLoS ONE 8, e61048.Google Scholar
Blasdell, K, Bordes, F, Chaisiri, K, Chaval, Y, Claude, J, Cosson, JF, Latinne, A, Michaux, J, Morand, S, Pagès, M and Tran, A (2015) Progress on research on rodents and rodent-borne zoonoses in South-East Asia. Wildlife Research 42, 98107.Google Scholar
Brooks, DR (1979) Testing the context and extent of host–parasite coevolution. Systematic Zoology 28, 299307.Google Scholar
Brooks, DR (1985) Historical ecology: a new approach to studying the evolution of associations. Annals of the Missouri Botanical Garden 72, 660680.Google Scholar
Chabé, M, Dei-Cas, E, Creusy, C, Fleurisse, L, Respaldiza, N, Camus, D and Durand-Joly, I (2004) Immunocompetent hosts as a reservoir of Pneumocystis organisms: histological and RT-PCR data demonstrate active replication. European Journal of Clinical Microbiology and Infectious Diseases 23, 8997.Google ScholarPubMed
Chabé, M, Herbreteau, V, Hugot, JP, Bouzard, N, Deruyter, L, Morand, S and Dei-Cas, E (2010) Pneumocystis carinii and Pneumocystis wakefieldiae in wild Rattus norvegicus trapped in Thailand. Journal of Eukaryotic Microbiology 57, 213217.Google Scholar
Chabé, M, Aliouat-Denis, C, Delhaes, L, Aliouat, EM, Viscogliosi, E and Dei-Cas, E (2011) Pneumocystis: from a doubtful unique entity to a group of highly diversified fungal species. FEMS Yeast Research 11, 217.CrossRefGoogle ScholarPubMed
Chaimanee, Y and Jaeger, J-J (2001) Evolution of Rattus (mammalia, Rodentia) during the Plio-Pleistocene in Thailand. Historical Biology 15, 181191.CrossRefGoogle Scholar
Conow, C, Fielder, D, Ovadia, Y and Libeskind-Hadas, R (2010) Jane: a new tool for the cophylogeny reconstruction problem. Algorithms for Molecular Biology 5, 16.CrossRefGoogle Scholar
Corbet, G and Hill, J (1992) The Mammals of the Indomalayan Region: A Systematic Review. Oxford: Oxford University Press.Google Scholar
Cushion, MT (1998) Genetic heterogeneity of rat-derived Pneumocystis. FEMS Immunology and Medical Microbiology 22, 5158.Google Scholar
Cushion, MT, Keely, SP and Stringer, JR (2004) Molecular and phenotypic description of Pneumocystis wakefieldiae sp. nov., a new species in rats. Mycologia 96, 429438.CrossRefGoogle Scholar
Danesi, P, da Rold, G, Rizzoli, A, Hauffe, HC, Marangon, S, Samerpitak, K, Demanche, C, Guillot, J, Capelli, G and de Hoog, SG (2016) Barcoding markers for Pneumocystis species in wildlife. Fungal Biology 120, 191206.CrossRefGoogle ScholarPubMed
De Vienne, DM, Giraud, T and Shykoff, JA (2007) When can host shifts produce congruent host and parasite phylogenies? A simulation approach. Journal of Evolutionary Biology 20, 14281438.CrossRefGoogle ScholarPubMed
De Vienne, DM, Refrégier, G, López-Villavicencio, M, Tellier, A, Hood, ME and Giraud, T (2013) Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytologist 198, 347385.Google Scholar
Dei-Cas, E, Chabé, M, Moukhlis, R, Durand-Joly, I, Aliouat, EM, Stringer, JR, Cushion, M, Noël, C, Sybren De Hoog, G, Guillot, J and Viscogliosi, E (2006) Pneumocystis oryctolagi sp. nov., an uncultured fungus causing pneumonia in rabbits at weaning: review of current knowledge, and description of a new taxon on genotypic, phylogenetic and phenotypic bases. FEMS Microbiology Reviews 30, 853871.CrossRefGoogle ScholarPubMed
Demanche, C, Berthelemy, M, Petit, T, Polack, B, Wakefield, AE, Dei-Cas, E and Guillot, J (2001) Phylogeny of Pneumocystis carinii from 18 primate species confirms host specificity and suggests coevolution. Journal of Clinical Microbiology 39, 21262133.Google Scholar
Demanche, C, Deville, M, Michaux, J, Barriel, V, Pinçon, C, Aliouat-Denis, CM, Pottier, M, Noël, C, Viscogliosi, E, Aliouat, EM, Dei-Cas, E, Morand, S and Guillot, J (2015) What Do Pneumocystis organisms tell us about the phylogeography of their hosts? The case of the woodmouse Apodemus sylvaticus in Continental Europe and Western Mediterranean Islands. PLoS ONE 10, e0120839.Google Scholar
Demanche, C, Deville, M, Michaux, J, Barriel, V, Pinçon, C, Aliouat-Denis, CM, Pottier, M, Noël, C, Viscogliosi, E, Aliouat, EM, Dei-Cas, E, Morand, S and Guillot, J (2017) Correction: what do Pneumocystis organisms tell us about the phylogeography of their hosts? The case of the woodmouse Apodemus sylvaticus in Continental Europe and Western Mediterranean Islands. PLoS ONE 12, e0171282.Google Scholar
Derouiche, S, Deville, M, Taylor, ML, Akbar, H, Guillot, J, Carreto-Binaghi, LE, Pottier, M, Aliouat, EM, Aliouat-Denis, CM, Dei-Cas, E and Demanche, C (2009) Pneumocystis diversity as a phylogeographic tool. Memórias do Instituto Oswaldo Cruz 104, 112117.Google Scholar
Desdevises, Y, Morand, S, Jousson, O and Legendre, P (2002) Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system. Evolution 56, 24592471.Google Scholar
Fabre, P-H, Pagès, M, Musser, GG, Fitriana, YS, Fjeldså, J, Jennings, A, Jønsson, KA, Kennedy, J, Michaux, J, Semiadi, G, Supriatna, N and Helgen, KM (2013) A new genus of rodent from Wallacea (Rodentia: Muridae: Murinae: Rattini), and its implication for biogeography and Indo-Pacific Rattini systematics. Zoological Journal of the Linnean Society 169, 408447.Google Scholar
Francis, CM (2008) A Field Guide to the Mammals of South-East Asia. London: New Holland.Google Scholar
Frenkel, JK (1999) Pneumocystis pneumonia, an immunodeficiency-dependent disease (IDD): a critical historical overview. Journal of Eukaryotic Microbiology 46, 89S92S.Google Scholar
Galan, M, Pagès, M and Cosson, J-F (2012) Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS ONE 7, e48374.Google Scholar
Gigliotti, F, Harmsen, AG, Haidaris, CG and Haidaris, PJ (1993) Pneumocystis carinii is not universally transmissible between mammalian species. Infection and Immunity 61, 28862890.Google Scholar
Giraud, T, Refrégier, G, Le Gac, M, de Vienne, DM and Hood, ME (2008) Speciation in fungi. Fungal Genetics and Biology 45, 791802.CrossRefGoogle ScholarPubMed
Guillot, J, Demanche, C, Hugot, JP, Berthelemy, M, Wakefield, AE, Dei-Cas, E and Chermette, R (2001) Parallel phylogenies of Pneumocystis species and their mammalian hosts. Journal of Eukaryotic Microbiology 48, 113S115S.CrossRefGoogle Scholar
Guillot, J, Demanche, C, Norris, K, Wildschutte, H, Wanert, F, Berthelemy, M, Tataine, S, Dei-Cas, E and Chermette, R (2004) Phylogenetic relationships among Pneumocystis from Asian macaques inferred from mitochondrial rRNA sequences. Molecular Phylogenetics and Evolution 31, 988996.Google Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3·0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hoberg, EP and Brooks, DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 15331550.Google Scholar
Hoberg, EP and Klassen, GJ (2002) Revealing the faunal tapestry: co-evolution and historical biogeography of hosts and parasites in marine systems. Parasitology 124, 322.Google Scholar
Hugot, JP, Demanche, C, Barriel, V, Dei-Cas, E and Guillot, J (2003) Phylogenetic systematics and evolution of primate-derived Pneumocystis based on mitochondrial or nuclear DNA sequence comparison. Systematic Biology 52, 735744.CrossRefGoogle ScholarPubMed
Hunter, JAC and Wakefield, AE (1996) Genetic divergence at the mitochondrial small subunit ribosomal RNA gene among isolates of Pneumocystis carinii from five mammalian host species. Journal of Eukaryotic Microbiology 43, 24S25S.Google Scholar
Icenhour, CR, Arnold, J, Medvedovic, M and Cushion, MT (2006) Competitive coexistence of two Pneumocystis species. Infection, Genetics and Evolution 6, 177186.Google Scholar
Janz, N and Nylin, S (2008) The oscillation hypothesis of host-plant range and speciation. In Tilmon, K (ed.). Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley: University of California Press, pp. 203215.Google Scholar
Kamiya, T, O'Dwyer, K, Nakagawa, S and Poulin, R (2014) Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37, 689697.Google Scholar
Keely, SP, Fischer, JM, Cushion, MT and Stringer, JR (2004) Phylogenetic identification of Pneumocystis murina sp. nov., a new species in laboratory mice. Microbiology 150, 11531165.CrossRefGoogle Scholar
Kimura, Y, Hawkins, MTR, McDonough, MM, Jacobs, LL and Flynn, LJ (2015) Corrected placement of Mus-Rattus fossil calibration forces precision in the molecular tree of rodents. Scientific Reports 5, 14444.Google Scholar
Latinne, A, Waengsothorn, S, Rojanadilok, P, Eiamampai, K, Sribuarod, K and Michaux, JR (2013) Diversity and endemism of Murinae rodents in Thai limestone karsts. Systematics and Biodiversity 11, 323344.Google Scholar
Legendre, P, Desdevises, Y and Bazin, E (2002) A statistical test for host–parasite coevolution. Systematic Biology 51, 217234.Google Scholar
Lekagul, B and McNeely, JA (1988) Mammals of Thailand. Bangkok: White Lotus Press.Google Scholar
Leung, TLF (2015) Fossils of parasites: what can the fossil record tell us about the evolution of parasitism? Biological Reviews 92, 410430.Google Scholar
Ma, L, Imamichi, H, Sukura, A and Kovacs, JA (2001) Genetic divergence of the dihydrofolate reductase and dihydropteroate synthase genes in Pneumocystis carinii from 7 different host species. Journal of Infectious Diseases 184, 13581362.Google Scholar
Martinez, A, Halliez, MCM, Moukhtar Aliouat, E, Chabé, M, Standaert-Vitse, A, Fréalle, E, Gantois, N, Pottier, M, Pinon, A, Dei-Cas, E and Aliouat-Denis, C-M (2013) Growth and airborne transmission of cell-sorted life cycle stages of Pneumocystis carinii. PLoS ONE 8, e79958.CrossRefGoogle ScholarPubMed
Mazars, E, Guyot, K, Fourmaintraux, S, Renaud, F, Petavy, F, Camus, D and Dei-Cas, E (1997) Detection of Pneumocystis in European wild animals. Journal of Eukaryotic Microbiology 44, 39s.Google Scholar
Meerburg, BG, Singleton, GR and Kijlstra, A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35, 221270.Google Scholar
Musser, GG and Carleton, M (2005) Superfamily Muroidea. In Wilson, DE and Reeder, DM (eds). Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore: Johns Hopkins University Press, pp. 8941531.Google Scholar
Pages, M, Chaval, Y, Herbreteau, V, Waengsothorn, S, Cosson, JF, Hugot, JP, Morand, S and Michaux, J (2010) Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evolutionary Biology 10, 184.Google Scholar
Pages, M, Bazin, E, Galan, M, Chaval, Y, Claude, J, Herbreteau, V, Michaux, JR, Piry, S, Morand, S and Cosson, JF (2013) Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex). Molecular Ecology 22, 10191034.CrossRefGoogle ScholarPubMed
Palmer, RJ, Cushion, MT and Wakefield, AE (1999) Discrimination of rat-derived Pneumocystis carinii f. sp. carinii and Pneumocystis carinii f. sp. ratti using the polymerase chain reaction. Molecular and Cellular Probes 13, 147155.Google Scholar
Palmer, RJ, Settnes, OP, Lodal, J and Wakefield, AE (2000) Population structure of rat-derived Pneumocystis carinii in Danish wild rats. Applied and Environmental Microbiology 66, 49544961.Google Scholar
Percy, DM, Page, RDM and Cronk, QCB (2004) Plant–insect interactions: double-dating associated insect and plant lineages reveals asynchronous radiations. Systematic Biology 53, 120127.Google Scholar
Posada, D (2008) Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.Google Scholar
R Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Rowe, KC, Aplin, KP, Baverstock, PR and Moritz, C (2011) Recent and rapid speciation with limited morphological disparity in the genus Rattus. Systematic Biology 60, 188203.Google Scholar
Schenk, JJ, Rowe, KC and Steppan, SJ (2013) Ecological opportunity and incumbency in the diversification of repeated continental colonizations by muroid rodents. Systematic Biology 62, 837864.Google Scholar
Stringer, JR, Cushion, M and Wakefield, AE (2001) New nomenclature for the genus Pneumocystis. Journal of Eukaryotic Microbiology 48, 184s189s.Google Scholar
Swofford, DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony, (*and Other Methods), version 4. Sunderland, MA: Sinauer Associates.Google Scholar
Tamura, K, Dudley, J, Nei, M and Kumar, S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Taylor, JW, Jacobson, DJ, Kroken, S, Kasuga, T, Geiser, DM, Hibbett, DS and Fisher, MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31, 2132.Google Scholar
Tsolaki, AG, Beckers, P and Wakefield, AE (1998) Pre-AIDS era isolates of Pneumocystis carinii f. sp. hominis: high genotypic similarity with contemporary isolates. Journal of Clinical Microbiology 36, 9093.Google Scholar
Wakefield, AE (1996) DNA sequences identical to Pneumocystis carinii f. sp. carinii and Pneumocystis carinii f. sp. hominis in samples of air spora. Journal of Clinical Microbiology 34, 17541759.Google Scholar
Wakefield, AE, Pixley, FJ, Banerji, S, Sinclair, K, Miller, RF, Moxon, ER and Hopkin, JM (1990) Detection of Pneumocystis carinii with DNA amplification. Lancet 336, 451453.Google Scholar
Wakefield, AE, Stringer, JR, Tamburrini, E and Dei-Cas, E (1998) Genetics, metabolism and host specificity of Pneumocystis carinii. Medical Mycology 36, 183193.Google Scholar
Supplementary material: File

Latinne et al supplementary material 1

Latinne et al supplementary material

Download Latinne et al supplementary material 1(File)
File 381.1 KB