Anidulafungin Treatment Blocks the Sexual Cycle of Pneumocystis murina and Prevents Growth and Survival without Rescue by an Alternative Mode of Replication.

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License: CC BY 4.0
Serval ID
serval:BIB_F2034698EFCC
Type
Article: article from journal or magazin.
Collection
Publications
Institution
Title
Anidulafungin Treatment Blocks the Sexual Cycle of Pneumocystis murina and Prevents Growth and Survival without Rescue by an Alternative Mode of Replication.
Journal
Microbiology spectrum
Author(s)
Cushion M.T., Ashbaugh A., Sayson S.G., Mosley C., Hauser P.M.
ISSN
2165-0497 (Electronic)
ISSN-L
2165-0497
Publication state
Published
Issued date
21/12/2022
Peer-reviewed
Oui
Volume
10
Number
6
Pages
e0290622
Language
english
Notes
Publication types: Journal Article
Publication Status: ppublish
Abstract
The proposed life cycle of fungi in the genus Pneumocystis has typically included both an asexual cycle via binary fission and a sexual cycle. Until recently, the strategy used for sexual replication was largely unknown, but genomic and functional assays now support a mode known as primary homothallism (self-fertilization). The question of whether an asexual cycle contributes to the growth of these fungi remains. Treatment of Pneumocystis pneumonia in immunosuppressed rodent models with the class of drugs known as echinocandins is challenging the historical concept of asexual replication. The echinocandins target 1,3-β-D-glucan (BG) synthesis resulting in death for most fungi. Because Pneumocystis species have both non-BG expressing life cycle stages (trophic forms) and BG-expressing asci, treatment with anidulafungin and caspofungin resulted in elimination of asci, with large numbers of non-BG expressing organisms remaining in the lungs. Transcriptional analyses of anidulafungin treated Pneumocystis murina-infected lungs indicated that these agents were blocking the sexual cycle. In the present study, we explored whether there was an asexual or alternative method of replication that could rescue P. murina survival and growth in the context of anidulafungin treatment. The effects of anidulafungin treatment on early events in the sexual cycle were investigated by RT-qPCR targeting specific mating genes, including mam2, map3, matMi, matPi, and matMc. Results from the in vivo and gene expression studies clearly indicated there was no rescue by an asexual cycle, supporting these fungi's reliance on the sexual cycle for survival and growth. Dysregulation of mating-associated genes showed that anidulafungin induced effects early in the mating process. IMPORTANCE The concept of a sexually obligate fungus is unique among human fungal pathogens. This reliance can be exploited for drug development and here we show a proof of principle for this unusual target. Most human fungal pathogens eschew the mammalian environment with its battery of immune responses. Pneumocystis appear to have evolved to survive in such an environment, perhaps by using sexual replication to help in DNA repair and to introduce genetic variation in its major surface antigen family because the lung is the primary environment of these pathogens. The concept of primary homothallism fits well into its chosen ecosystem, with ready mating partners expressing both mating type receptors, and a sexual cycle that can introduce beneficial genetic variation without the need for outbreeding.
Keywords
Animals, Humans, Anidulafungin/therapeutic use, Ecosystem, Pneumocystis/genetics, Pneumonia, Pneumocystis/drug therapy, Echinocandins/pharmacology, Echinocandins/therapeutic use, Mammals, Pneumocystis, Pneumocystis pneumonia, asci, echinocandin, echinocandins, fungal asexual reproduction, fungal sexual reproduction
Pubmed
Open Access
Yes
Create date
02/11/2022 8:22
Last modification date
23/01/2024 7:37
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