Phylogenetic systematics and evolution of primate-derived Pneumocystis based on mitochondrial or nuclear DNA sequence comparison.

Previous studies have demonstrated that the agent of Pneumocystis pneumonia (PcP), Pneumocystis carinii, is actually a complex of eukaryotic organisms, and cophylogeny could explain the distribution of the hosts and parasites. In the present work, we tested the hypothesis of cophylogeny between the primate-derived Pneumocystis group and their hosts. Specific strains isolated from 20 primate species, including humans, were used to produce a phylogeny of the parasites. Aligned sequences corresponding to DNA sequences of three genes (DHPS, mtSSU-rRNA, and mtLSU-rRNA) were separately analyzed and then combined in a single data set. The resulting parasite phylogeny was compared with different controversial phylogenies for the hosts. This comparison demonstrated that, depending upon which topology is accepted for the hosts, at least 61% and perhaps 77% of the homologous nodes of the respective cladograms of the hosts and parasites may be interpreted as resulting from codivergence events. This finding and the high specificity of these parasites suggests that cophylogeny may be considered the dominant pattern of evolution for Pneumocystis organisms, representing a new example of parallel evolution between primates and their specific parasites. Because the phylogeny of Pneumocystis followed very closely the differentiation of their hosts at the species level, the study of the parasites could provide valuable information on the phylogeny of their hosts. We used this information to explore controversial hypotheses of the phylogeny of the Platyrrhini by comparison with the phylogeny of their specific Pneumocystis parasites. If these organisms were closely associated as lung parasites with primates through the ages, the hypothesis of the Pneumocystis spp. being new pathogenic agents could be refuted. However, these organisms are opportunistic symbionts, becoming pathogenic whenever the immunological defences of their hosts decline. This study also provides support for the hypothesis that the different Pneumocystis species are genetically independent organisms, helping to clarify their taxonomic status.

[1]  R. Page,et al.  When do parasites fail to speciate in response to host speciation? , 2003, Systematic biology.

[2]  J. Stringer,et al.  Pneumocystis carinii: what is it, exactly? , 1996, Clinical microbiology reviews.

[3]  A. Purvis A composite estimate of primate phylogeny. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  M. Goodman,et al.  DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes. , 1995, Molecular phylogenetics and evolution.

[5]  E. Dei‐Cas,et al.  Pneumocystis cross infection experiments using SCID mice and nude rats as recipient host, showed strong host-species specificity. , 1994, The Journal of eukaryotic microbiology.

[6]  M. Goodman,et al.  The place of Callimico goeldii in the Callitrichine phylogenetic tree: evidence from von Willebrand factor gene intron II sequences. , 1999, Molecular phylogenetics and evolution.

[7]  M. A. Moreira,et al.  Can molecular data place each neotropical monkey in its own branch? , 2001, Chromosoma.

[8]  C. Haidaris,et al.  Pneumocystis carinii is not universally transmissible between mammalian species , 1993, Infection and immunity.

[9]  J. Hugot Primates and their pinworm parasites: the cameron hypothesis revisited. , 1999, Systematic biology.

[10]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[11]  E Dei-Cas Pneumocystis infections: the iceberg? , 2000, Medical mycology.

[12]  M. Goodman,et al.  Molecular phylogeny of the New World monkeys (Platyrrhini, primates) based on two unlinked nuclear genes: IRBP intron 1 and epsilon-globin sequences. , 1996, American journal of physical anthropology.

[13]  R. Page,et al.  Comparative analysis of secondary structure of insect mitochondrial small subunit ribosomal RNA using maximum weighted matching. , 2000, Nucleic acids research.

[14]  Roderic D. M. Page,et al.  PARALLEL PHYLOGENIES: RECONSTRUCTING THE HISTORY OF HOST‐PARASITE ASSEMBLAGES , 1994 .

[15]  A. Rosenberger Fossil New World monkeys dispute the molecular clock , 1984 .

[16]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[17]  R. Barros,et al.  Cytogenetic study of the genus Saguinus (Callithrichidae, Primates) , 1997 .

[18]  E. Angeli,et al.  P.carinii host specificity: attempt of cross infections with human derived strains in rats. , 1999, The Journal of eukaryotic microbiology.

[19]  E. Dei‐Cas,et al.  Pneumocystis carinii f. sp. hominis Is Not Infectious for SCID mice , 2002, Journal of Clinical Microbiology.

[20]  J. Stringer,et al.  Genetics, metabolism and host specificity of Pneumocystis carinii. , 1998, Medical mycology.

[21]  Frenkel Jk Pneumocystis jiroveci n. sp. from man: morphology, physiology, and immunology in relation to pathology. , 1976 .

[22]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[23]  J. Hugot,et al.  Evolution of the Old World Arenaviridae and their rodent hosts: generalized host-transfer or association by descent? , 2001, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[24]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[25]  J. Hugot Phylogeny of neotropical monkeys: the interplay of morphological, molecular, and parasitological data. , 1998, Molecular phylogenetics and evolution.

[26]  R. Kay,et al.  The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea) , 1990 .

[27]  F. Barré-Sinoussi,et al.  Simian Immunodeficiency Viruses and the Origin of HIVs , 2002 .

[28]  J. Cesbron,et al.  Intranasal Inoculation of Mouse, Rat or Rabbit-Derived Pneumocystis to SCID Mice , 1993 .

[29]  M. Sogin,et al.  Ribosomal RNA sequence shows Pneumocystis carinii to be a member of the Fungi , 1988, Nature.

[30]  P. Gill DNA evidence , 1995, Nature.

[31]  M. Goodman,et al.  Molecular phylogeny of the New World monkeys (Platyrrhini, primates). , 1993, Molecular phylogenetics and evolution.

[32]  C. Simon,et al.  The performance of several multiple-sequence alignment programs in relation to secondary-structure features for an rRNA sequence. , 2000, Molecular biology and evolution.

[33]  J. Cheverud,et al.  Historical biogeography of tamarins, genus Saguinus: the molecular phylogenetic evidence. , 1999, American journal of physical anthropology.

[34]  I. Ricard,et al.  Ultrastructural and molecular characterization of Pneumocystis carinii isolated from a rhesus monkey (Macaca mulatta). , 2000, Medical mycology.

[35]  M. Goodman,et al.  Phylogeny and Evolution of Selected Primates as Determined by Sequences of the ε-Globin Locus and 5′ Flanking Regions , 1997, International Journal of Primatology.

[36]  J. Stringer,et al.  New Nomenclature for the Genus Pneumocystis , 2001, The Journal of eukaryotic microbiology.

[37]  T. Sata,et al.  Severe pulmonary pneumocystosis in simian acquired immunodeficiency syndrome induced by simian immunodeficiency virus: its characterization by the polymerase-chain-reaction method and failure of experimental transmission to immunodeficient animals , 2004, Parasitology Research.

[38]  J. K. Frenkel,et al.  Pneumocystis pneumonia, an immunodeficiency-dependent disease (IDD): a critical historical overview. , 1999, The Journal of eukaryotic microbiology.

[39]  D. Maddison,et al.  MacClade 4: analysis of phy-logeny and character evolution , 2003 .

[40]  E. Dei‐Cas,et al.  Phylogeny of Pneumocystis carinii from 18 Primate Species Confirms Host Specificity and Suggests Coevolution , 2001, Journal of Clinical Microbiology.

[41]  C. Groves,et al.  Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. , 1998, Molecular phylogenetics and evolution.

[42]  M. Siddall,et al.  The AIDS Pandemic is New, but is HIVNotNew?☆☆☆ , 1997 .

[43]  P. Parham,et al.  Molecular phylogeny of new world primates (Platyrrhini) based on beta2-microglobulin DNA sequences. , 1999, Molecular phylogenetics and evolution.

[44]  J. K. Frenkel Pneumocystis jiroveci n. sp. from man: morphology, physiology, and immunology in relation to pathology. , 1976, National Cancer Institute monograph.

[45]  J. Hugot,et al.  Parallel Phylogenies of Pneumocystis Species and their Mammalian Hosts , 2001, The Journal of eukaryotic microbiology.

[46]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[47]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[48]  A. Gorbalenya,et al.  Topley and Wilson's Microbiology and Microbial Infections , 2005 .

[49]  M. Ruvolo,et al.  Phylogenetic relationships of the New World monkeys (Primates, platyrrhini) based on nuclear G6PD DNA sequences. , 1999, Molecular phylogenetics and evolution.

[50]  A. Meyer,et al.  Systematics of New World monkeys (Platyrrhini, Primates) based on 16S mitochondrial DNA sequences: a comparative analysis of different weighting methods in cladistic analysis. , 1995, Molecular phylogenetics and evolution.

[51]  V. Barriel,et al.  Phylogénies moléculaires et insertions-délétions de nucléotides , 1994 .