Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors

ABSTRACT The genus Pneumocystis encompasses fungal species that colonize mammals’ lungs with host specificity. Should the host immune system weaken, the fungal species can cause severe pneumonia. The life cycle of these pathogens is poorly known, mainly because an in vitro culture method has not bee...

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Autores principales:	A. Luraschi, S. Richard, J. M. G. C. F. Almeida, M. Pagni, M. T. Cushion, P. M. Hauser
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	homothallism opportunistic fungi sexuality Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/443a75d9c0ab4409a6553a0b4a534668
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spelling	oai:doaj.org-article:443a75d9c0ab4409a6553a0b4a5346682021-11-15T16:22:11ZExpression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors10.1128/mBio.01145-192150-7511https://doaj.org/article/443a75d9c0ab4409a6553a0b4a5346682019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01145-19https://doaj.org/toc/2150-7511ABSTRACT The genus Pneumocystis encompasses fungal species that colonize mammals’ lungs with host specificity. Should the host immune system weaken, the fungal species can cause severe pneumonia. The life cycle of these pathogens is poorly known, mainly because an in vitro culture method has not been established. Both asexual and sexual cycles would occur. Trophic cells, the predominant forms during infection, could multiply asexually but also enter into a sexual cycle. Comparative genomics revealed a single mating type locus, including plus and minus genes, suggesting that primary homothallism involving self-fertility of each strain is the mode of reproduction of Pneumocystis species. We identified and analyzed the expression of the mam2 and map3 genes encoding the receptors for plus and minus pheromones using reverse transcriptase PCR, in both infected mice and bronchoalveolar lavage fluid samples from patients with Pneumocystis pneumonia. Both receptors were most often concomitantly expressed during infection, revealing that both pheromone-receptor systems are involved in the sexual cycle. The map3 transcripts were subject to alternative splicing. Using immunostaining, we investigated the presence of the pheromone receptors at the surfaces of Pneumocystis cells from a patient. The staining tools were first assessed in Saccharomyces cerevisiae displaying the Pneumocystis receptors at their cellular surface. Both receptors were present at the surfaces of the vast majority of the cells that were likely trophic forms. The receptors might have a role in mate recognition and/or postfertilization events. Their presence at the cell surface might facilitate outbreeding versus inbreeding of self-fertile strains. IMPORTANCE The fungi belonging to the genus Pneumocystis may cause severe pneumonia in immunocompromised humans, a disease that can be fatal if not treated. This disease is nowadays one of the most frequent invasive fungal infections worldwide. Whole-genome sequencing revealed that the sexuality of these fungi involves a single partner that can self-fertilize. Here, we report that two receptors recognizing specifically excreted pheromones are involved in this self-fertility within infected human lungs. Using fluorescent antibodies binding specifically to these receptors, we observed that most often, the fungal cells display both receptors at their surface. These pheromone-receptor systems might play a role in mate recognition and/or postfertilization events. They constitute an integral part of the Pneumocystis obligate sexuality within human lungs, a cycle that is necessary for the dissemination of the fungus to new individuals.A. LuraschiS. RichardJ. M. G. C. F. AlmeidaM. PagniM. T. CushionP. M. HauserAmerican Society for Microbiologyarticlehomothallismopportunistic fungisexualityMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	homothallism opportunistic fungi sexuality Microbiology QR1-502
spellingShingle	homothallism opportunistic fungi sexuality Microbiology QR1-502 A. Luraschi S. Richard J. M. G. C. F. Almeida M. Pagni M. T. Cushion P. M. Hauser Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors
description	ABSTRACT The genus Pneumocystis encompasses fungal species that colonize mammals’ lungs with host specificity. Should the host immune system weaken, the fungal species can cause severe pneumonia. The life cycle of these pathogens is poorly known, mainly because an in vitro culture method has not been established. Both asexual and sexual cycles would occur. Trophic cells, the predominant forms during infection, could multiply asexually but also enter into a sexual cycle. Comparative genomics revealed a single mating type locus, including plus and minus genes, suggesting that primary homothallism involving self-fertility of each strain is the mode of reproduction of Pneumocystis species. We identified and analyzed the expression of the mam2 and map3 genes encoding the receptors for plus and minus pheromones using reverse transcriptase PCR, in both infected mice and bronchoalveolar lavage fluid samples from patients with Pneumocystis pneumonia. Both receptors were most often concomitantly expressed during infection, revealing that both pheromone-receptor systems are involved in the sexual cycle. The map3 transcripts were subject to alternative splicing. Using immunostaining, we investigated the presence of the pheromone receptors at the surfaces of Pneumocystis cells from a patient. The staining tools were first assessed in Saccharomyces cerevisiae displaying the Pneumocystis receptors at their cellular surface. Both receptors were present at the surfaces of the vast majority of the cells that were likely trophic forms. The receptors might have a role in mate recognition and/or postfertilization events. Their presence at the cell surface might facilitate outbreeding versus inbreeding of self-fertile strains. IMPORTANCE The fungi belonging to the genus Pneumocystis may cause severe pneumonia in immunocompromised humans, a disease that can be fatal if not treated. This disease is nowadays one of the most frequent invasive fungal infections worldwide. Whole-genome sequencing revealed that the sexuality of these fungi involves a single partner that can self-fertilize. Here, we report that two receptors recognizing specifically excreted pheromones are involved in this self-fertility within infected human lungs. Using fluorescent antibodies binding specifically to these receptors, we observed that most often, the fungal cells display both receptors at their surface. These pheromone-receptor systems might play a role in mate recognition and/or postfertilization events. They constitute an integral part of the Pneumocystis obligate sexuality within human lungs, a cycle that is necessary for the dissemination of the fungus to new individuals.
format	article
author	A. Luraschi S. Richard J. M. G. C. F. Almeida M. Pagni M. T. Cushion P. M. Hauser
author_facet	A. Luraschi S. Richard J. M. G. C. F. Almeida M. Pagni M. T. Cushion P. M. Hauser
author_sort	A. Luraschi
title	Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors
title_short	Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors
title_full	Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors
title_fullStr	Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors
title_full_unstemmed	Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors
title_sort	expression and immunostaining analyses suggest that <italic toggle="yes">pneumocystis</italic> primary homothallism involves trophic cells displaying both plus and minus pheromone receptors
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/443a75d9c0ab4409a6553a0b4a534668
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Expression and Immunostaining Analyses Suggest that <italic toggle="yes">Pneumocystis</italic> Primary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors

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