Genomics and evolution of Pneumocystis species

Abstract

The genus Pneumocystis comprises highly diversified fungal species that cause severe pneumonia in individuals with a deficient immune system. These fungi infect exclusively mammals and present a strict host species specificity. These species have co-diverged with their hosts for long periods of time (> 100 MYA). Details of their biology and evolution are fragmentary mainly because of a lack of an established long-term culture system. Recent genomic advances have unlocked new areas of research and allow new hypotheses to be tested. We review here new findings of the genomic studies in relation with the evolutionary trajectory of these fungi and discuss the impact of genomic data analysis in the context of the population genetics. The combination of slow genome decay and limited expansion of specific gene families and introns reflect intimate interactions of these species with their hosts. The evolutionary adaptation of these organisms is profoundly influenced by their population structure, which in turn is determined by intrinsic features such as their self-fertilizing mating system, high host specificity, long generation times, and transmission mode. Essential key questions concerning their adaptation and speciation remain to be answered. The next cornerstone will consist in the establishment of a long-term culture system and genetic manipulation that should allow unravelling the driving forces of Pneumocystis species evolution.

Decades-old studies of fungi associated with mammalian lungs and modern DNA sequencing approaches help define the nature of the lung mycobiome

“…Perhaps the most exquisitely adapted members of lung mycobiomes, species of Pneumocystis are widespread among mammals, are specifically adapted to lung tissues, and exhibit host specificity. Co-evolution between mammalian hosts and species of Pneumocystis has been shown for humans, nonhuman primates, and bats [32][33][34]. Studies of such Pneumocystis-host associations have the potential to provide insights for transmission, phylogenetic relationships, and cell biology.…”

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

“…Genomic and phenotypic divergence made possible the description of several Pneumocystis species [17][18][19][20] such that at the end of the 20th century, the unique taxonomically enigmatic entity called "Pneumocystis carinii" suddenly became a group of stenoxenic species. Another aspect of host specificity is that Pneumocystis species are mostly obligate biotrophs [9,[21][22][23]. Indeed, Pneumocystis organisms secrete low amounts of lytic proteases and cause little damage to their hosts.…”

“…Indeed, Pneumocystis organisms secrete low amounts of lytic proteases and cause little damage to their hosts. These are two hallmarks of biotrophy, where, in a parasitic relationship, the parasite obtains food from living host cells [21,23]. Moreover, most biotrophs are obligate parasites, meaning they cannot survive without their hosts and cannot be cultured axenically in the laboratory [24].…”

Genotyping Pneumocystis jirovecii: Impacting Our Understanding of Interhuman Transmission

“…RFLP analysis targeting the major surface glycoprotein family A1 gene (msg-RFLP) was proposed in 2009 and successfully used to investigate outbreaks in two centers receiving renal transplant patients [32,33]. The msg-RFLP assay targets a 1300 bp fragment of the A1 msg gene subfamily, which is described as highly polymorphic [14,34,35]. This method was also used in addition to a multilocus sequence typing (MLST) scheme of 3 loci to investigate an outbreak in a Danish transplant center [36].…”

“…Most of these questions can be addressed using genotyping, which must be performed directly on clinical specimens because of the absence of reliable culture methods [12]. P. jirovecii genotyping strategies have been debated in several reviews [13,14]. Recently, Alanio et al also proposed a review on fungi genotyping strategies with a focus on P. jirovecii [15].…”