Pondering Mating: Pneumocystis jirovecii, the Human Lung Pathogen, Selfs without Mating Type Switching, in Contrast to Its Close Relative Schizosaccharomyces pombe

Inderbitzin, Patrik; Turgeon, B. Gillian

doi:10.1128/mbio.00583-15

Cited by 5 publications

(6 citation statements)

References 42 publications

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“…At the cellular level there are two very different forms of homothallism: primary and secondary (Lin and Heitman 2007; Almeida et al 2015; Inderbitzin and Turgeon 2015; Wilson et al 2015). In primary homothallic species, any cell can mate with any other cell.…”

Section: Heterothallism and Two Types Of Homothallismmentioning

confidence: 99%

“…The definition of homothallism becomes more finessed when applied to cells instead of strains, which is crucial for yeasts because they are unicellular organisms. At the cellular level there are two very different forms of homothallism: primary and secondary ( Lin and Heitman 2007 ; Almeida et al 2015 ; Inderbitzin and Turgeon 2015 ; Wilson et al 2015 ). In primary homothallic species, any cell can mate with any other cell.…”

Section: Heterothallism and Two Types Of Homothallismmentioning

confidence: 99%

“…In contrast, surprisingly little is known about the molecular basis of primary homothallism. In Pezizomycotina, primary homothallics such as some Cochliobolus species have a single type of MAT locus containing genes normally found in both alleles, whose structures indicate that they were formed by recombination between MAT chromosomes of heterothallic ancestors ( Yun et al 1999 ; Inderbitzin and Turgeon 2015 ). In Taphrinomycotina, it has recently been proposed that the pathogen Pneumocystis is a primary homothallic because it too has MAT genes from both alleles in close proximity on the same chromosome ( Almeida et al 2015 ).…”

Section: Heterothallism and Two Types Of Homothallismmentioning

confidence: 99%

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An Evolutionary Perspective on Yeast Mating-Type Switching

2017

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Cell differentiation in yeast species is controlled by a reversible, programmed DNA-rearrangement process called mating-type switching. Switching is achieved by two functionally similar but structurally distinct processes in the budding yeast Saccharomyces cerevisiae and the fission yeast Schizosaccharomyces pombe. In both species, haploid cells possess one active and two silent copies of the mating-type locus (a three-cassette structure), the active locus is cleaved, and synthesis-dependent strand annealing is used to replace it with a copy of a silent locus encoding the opposite mating-type information. Each species has its own set of components responsible for regulating these processes. In this review, we summarize knowledge about the function and evolution of mating-type switching components in these species, including mechanisms of heterochromatin formation, MAT locus cleavage, donor bias, lineage tracking, and environmental regulation of switching. We compare switching in these well-studied species to others such as Kluyveromyces lactis and the methylotrophic yeasts Ogataea polymorpha and Komagataella phaffii. We focus on some key questions: Which cells switch mating type? What molecular apparatus is required for switching? Where did it come from? And what is the evolutionary purpose of switching?

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Section: Heterothallism and Two Types Of Homothallismmentioning

confidence: 99%

Section: Heterothallism and Two Types Of Homothallismmentioning

confidence: 99%

Section: Heterothallism and Two Types Of Homothallismmentioning

confidence: 99%

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An Evolutionary Perspective on Yeast Mating-Type Switching

2017

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“…Instead, any strain can mate with any other strain. Two major forms of homothallism are recognized-primary and secondary-with mating-type switching occurring only in secondary homothallics [2,3,8]. In primary homothallic species, it is thought that any cell can mate with any other cell, though this has not been investigated in detail [5].…”

Section: Resultsmentioning

confidence: 99%

Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution

et al. 2019

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Summary Cell type in budding yeasts is determined by the genotype at the mating-type ( MAT ) locus, but yeast species differ widely in their mating compatibility systems and life cycles. Among sexual yeasts, heterothallic species are those in which haploid strains fall into two distinct and stable mating types ( MATa and MAT α), whereas homothallic species are those that can switch mating types or that appear not to have distinct mating types [ 1 , 2 ]. The evolutionary history of these mating compatibility systems is uncertain, particularly regarding the number and direction of transitions between homothallism and heterothallism, and regarding whether the process of mating-type switching had a single origin [ 3 , 4 , 5 ]. Here, we inferred the mating compatibility systems of 332 budding yeast species from their genome sequences. By reference to a robust phylogenomic tree [ 6 ], we detected evolutionary transitions between heterothallism and homothallism, and among different forms of homothallism. We find that mating-type switching has arisen independently at least 11 times during yeast evolution and that transitions from heterothallism to homothallism greatly outnumber transitions in the opposite direction (31 versus 3). Although the 3-locus MAT-HML-HMR mechanism of mating-type switching as seen in Saccharomyces cerevisiae had a single evolutionary origin in budding yeasts, simpler “flip/flop” mechanisms of switching evolved separately in at least 10 other groups of yeasts. These results point to the adaptive value of homothallism and mating-type switching to unicellular fungi.

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“…S. pombe harbors MAT transcription factors with homeobox or high-motility-group (HMG) DNA binding domains. Consequently, our searches using S. pombe MAT genes as sequence queries ( 17 ) could not identify MAT transcription factors with MAT α 1 or amphipathic alpha-helix domains that are present in ascomycetous subphyla other than Taphrinomycotina, such as Saccharomycotina and Pezizomycotina ( 19 ). Extensive homology searches using tBLASTn involving bait sequences recruited through InterPro references did not detect any such transcription factors in the P. jirovecii and P. carinii genomes or in that of Pneumocystis murina , the species that infects mice.…”

Section: Resultsmentioning

confidence: 99%

Functional and Expression Analyses of the Pneumocystis MAT Genes Suggest Obligate Sexuality through Primary Homothallism within Host Lungs

Richard

Almeida

Cissé

et al. 2018

mBio

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Fungi of the genus Pneumocystis are obligate parasites that colonize mammals’ lungs and are host species specific. Pneumocystis jirovecii and Pneumocystis carinii infect, respectively, humans and rats. They can turn into opportunistic pathogens in immunosuppressed hosts, causing severe pneumonia. Their cell cycle is poorly known, mainly because of the absence of an established method of culture in vitro. It is thought to include both asexual and sexual phases. Comparative genomic analysis suggested that their mode of sexual reproduction is primary homothallism involving a single mating type (MAT) locus encompassing plus and minus genes (matMc, matMi, and matPi; Almeida et al., mBio 6:e02250-14, 2015). Thus, each strain would be capable of sexual reproduction alone (self-fertility). However, this is a working hypothesis derived from computational analyses that is, in addition, based on the genome sequences of single isolates. Here, we tested this hypothesis in the wet laboratory. The function of the P. jirovecii and P. carinii matMc genes was ascertained by restoration of sporulation in the corresponding mutant of fission yeast. Using PCR, we found the same single MAT locus in all P. jirovecii isolates and showed that all three MAT genes are often concomitantly expressed during pneumonia. Extensive homology searches did not identify other types of MAT transcription factors in the genomes or cis-acting motifs flanking the MAT locus that could have been involved in MAT switching or silencing. Our observations suggest that Pneumocystis sexuality through primary homothallism is obligate within host lungs to complete the cell cycle, i.e., produce asci necessary for airborne transmission to new hosts.

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Pondering Mating: Pneumocystis jirovecii, the Human Lung Pathogen, Selfs without Mating Type Switching, in Contrast to Its Close Relative Schizosaccharomyces pombe

Cited by 5 publications

References 42 publications

An Evolutionary Perspective on Yeast Mating-Type Switching

An Evolutionary Perspective on Yeast Mating-Type Switching

Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution

Functional and Expression Analyses of the Pneumocystis MAT Genes Suggest Obligate Sexuality through Primary Homothallism within Host Lungs

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