Phylogenetic Systematics and Evolution of Primate-Derived Pneumocystis Based on Mitochondrial or Nuclear DNA Sequence Comparison

Abstract

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.

Characterizing Pneumocystis in the Lungs of Bats: Understanding Pneumocystis Evolution and the Spread of Pneumocystis Organisms in Mammal Populations

“…This view is further consistent with the fine adaptation of Pneumocystis organisms to the alveolar microenvironment (8,16,23,26), likely resulting from Pneumocystis-host species coevolution (46). Consistently, it was experimentally shown that Pneumocystis organisms were able to replicate in the lungs of healthy hosts (16), which can subsequently transmit the microfungi by airborne route to susceptible or immunocompetent hosts (32,39).…”

“…Indeed, the narrow host specificity of Pneumocystis species emerged clearly from the failure of cross species infection among laboratory animals (1,38) or between humans and SCID mice (33). Surveys in domestic, synanthropic, or wild species showed that mammals may harbor one or several host-specific Pneumocystis species or strains (3,17,27,31,41,46).…”

“…However, ultrastructure (25,99), short-term culture (2,19), and cell sorting approaches (56,57) led to quite heuristic life cycle hypotheses. Furthermore, using PcP animal models, molecular strategies and the exploring of Pneumocystis occurrence in wild mammals resulted in major advancements, like the notions of strong host species specificity (1,27,31,33,38,41) and coevolution (3,27,31,46). Bats (Chiroptera) are widely distributed across various ecosystems and constitute one of the largest groups of mammals, second in number of species after the order Rodentia and first in number of individuals (69).…”

La transmission des infections àPneumocystis

“…De nos jours, la pneumocystose reste [10]. De plus, les études récentes sur la coévolution des Pneumocystis et de leurs hôtes témoignent de l'adaptation très ancienne de ces parasites aux mammifères [11,12]. Ainsi, le genre Pneumocystis regroupe des populations génétiquement isolées, qui ont subi un long processus d'adaptation à chaque espèce de mammifère, entraînant une spé-ciation [10].…”

Rising incidence of Pneumocystis jirovecii pneumonia suggests iatrogenic exposure of immune-compromised patients may be becoming a significant problem

“…Pneumocystis jirovecii, originally classified as a protozoan, was reclassified in 1999 as a fungus in the phylum Ascomycota (Hugot et al, 2003) on the basis of DNA and protein analysis (Stringer et al, 2002). While it is an obligate human parasite of the human respiratory tract, its DNA can be found in airborne fungal spores (Wakefield, 1996), increasing the risk of environmental exposure.…”