Pneumocystis Species Co-evolution: State-of-the-Art Review

Abstract

Pneumocystis spp. are a group of fungi that are known for causing opportunistic infections in immunocompromised individuals. It was only at the end of the 20th century that the scientific community challenged the notion of a unique species in the genus Pneumocystis (i.e., Pneumocystis carinii) that drastically changed the understanding of the natural history of pneumocystosis. It is now accepted that the Pneumocystis genus comprises a group of heterogenous fungi having multiple stenoxenic biological entities. These are widely distributed in the ecosystems and closely adapt to the mammalian species they colonize. The infection is transmitted via airborne route, allowing them to successfully dwell in the lungs of infected individuals. This article reviews some of the atypical features of these fungal microorganisms, namely host specificity and their parallel history with the mammalian hosts in which they co-evolve. Pneumocystis organisms can serve as powerful tools for phylogenetic and phylogeographic studies in mammals. Finally, the review challenges the genetic markers used historically to study the genetic diversity of

Rethinking host range in Pneumocystis

“…The same phenomenon is observed in bats [9], often cited as the best example of highly hostspecific Pneumocystis [e.g. 2,15,18]. In the only instance of successful intrageneric Pneumocystis sampling in bats, mtSSU was sequenced from two species of long-eared bat, Plecotus auritus and P. austriacus, and found to be only 0.49% divergent [9].…”

“…Certainly, these data are incomplete and reveal no hard truths about Pneumocystis host specificity, especially given the challenges of basing hypotheses on limited mitochondrial data from a limited number of host species. However, no experimental or genetic evidence has conclusively demonstrated single-host specificity in Pneumocystis, although this claim continues to be repeated [1,2]. Pneumocystis is poorly sampled, with thousands of mammal host species untested; that we have already encountered many probable exceptions to monoxenism suggests that multihost range is not rare.…”

“…However, only a small percentage of mammal species have been tested for Pneumocystis, and only five Pneumocystis species have been formally described. Despite our massive knowledge gaps, the notion of monoxenism in Pneumocystis is so pervasive that evidence to the contrary is often described as rare exceptions to a rule [1,2]. Here, we review the literature on host distribution of Pneumocystis and argue that monoxenism is not supported by the available, albeit limited, data.…”

“…More surprisingly, the red spiny rat (Maxomys surifer) and Herbert's giant rat (Leopoldamys herberti), which are separated by approximately 7 million years of evolution [10], were found to harbor identical Pneumocystis genetic sequences [15]. Nevertheless, the notion of monoxenism has persisted, and cases such as these are described as rare potential exceptions [1,2]. However, these findings suggest that host range is constrained by host divergence time rather than the speciation process per se, which leads us to scrutinize the evidence used to conclude that Pneumocystis species are primarily monoxenous.…”

“…Fungi in the genus Pneumocystis are obligate biotrophs and opportunistic pathogens of mammal lungs. They are notable for their high degree of host specificity; it is often argued that Pneumocystis species are restricted to a single host species (i.e., monoxenous) [1,2]. This monoxenous hypothesis, combined with their ubiquitous presence across mammal diversity, suggests that there may be one Pneumocystis species for each of the 6399 extant mammal species.…”