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Discovery of a phenotypic switch regulating sexual mating in the opportunistic fungal pathogen Candida tropicalis

ABSTRACT: Sexual reproduction can promote genetic diversity in eukaryotes, and yet many pathogenic fungi have been labeled as obligate asexual species. It is becoming increasingly clear, however, that cryptic sexual programs may exist in some species, and that efficient mating requires the necessary developmental switch to be triggered. In this study we investigate Candida tropicalis, an important human fungal pathogen that has been reported to be asexual. Significantly, we demonstrate that C. tropicalis uses a phenotypic switch to regulate a cryptic program of sexual mating. Thus, diploid a and α cells must undergo a developmental transition to the mating-competent form, and only then does efficient cell-cell conjugation take place resulting in the formation of stable a/α tetraploids. We show that both the phenotypic switch and sexual mating depend on the conserved transcriptional regulator Wor1, which is regulated by temperature in other fungal species. In contrast, C. tropicalis mating occurs efficiently at both 25 °C and 37 °C, suggesting that it could occur in the mammalian host and have direct consequences for the outcome of an infection. Transcriptional profiling further reveals that ≈400 genes are differentially expressed between the two phenotypic states, including the regulatory factor Wor1. Taken together, our results demonstrate that C. tropicalis has a unique sexual program, and that entry to this program is controlled via a Wor1-mediated, metastable switch. These observations have direct implications for the regulation and evolution of cryptic sexual programs in related fungal pathogens.

ORGANISM(S): Candida tropicalis

PROVIDER: GSE40179 | GEO | 2012/08/28

SECONDARY ACCESSION(S): PRJNA173866

REPOSITORIES: GEO

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Discovery of a phenotypic switch regulating sexual mating in the opportunistic fungal pathogen Candida tropicalis

Project description:Sexual reproduction can promote genetic diversity in eukaryotes, and yet many pathogenic fungi have been labeled as obligate asexual species. It is becoming increasingly clear, however, that cryptic sexual programs may exist in some species, and that efficient mating requires the necessary developmental switch to be triggered. In this study we investigate Candida tropicalis, an important human fungal pathogen that has been reported to be asexual. Significantly, we demonstrate that C. tropicalis uses a phenotypic switch to regulate a cryptic program of sexual mating. Thus, diploid a and α cells must undergo a developmental transition to the mating-competent form, and only then does efficient cell-cell conjugation take place resulting in the formation of stable a/α tetraploids. We show that both the phenotypic switch and sexual mating depend on the conserved transcriptional regulator Wor1, which is regulated by temperature in other fungal species. In contrast, C. tropicalis mating occurs efficiently at both 25 °C and 37 °C, suggesting that it could occur in the mammalian host and have direct consequences for the outcome of an infection. Transcriptional profiling further reveals that ≈400 genes are differentially expressed between the two phenotypic states, including the regulatory factor Wor1. Taken together, our results demonstrate that C. tropicalis has a unique sexual program, and that entry to this program is controlled via a Wor1-mediated, metastable switch. These observations have direct implications for the regulation and evolution of cryptic sexual programs in related fungal pathogens. 4 biological replicates of both the white (CAY1504) and opaque (CAY2275) states of C. tropicalis a cells are included on this array. All are hybridized against a universal reference sample, which consists of the combined RNA from all 8 replicates used on this array.

2012-08-28 | E-GEOD-40179 | biostudies-arrayexpress

The gray phenotype in the human fungal pathogen Candida tropicalis

Project description:Phenotypic plasticity, the ability to switch between different morphological types, plays critical roles in environmental adaptation, leading to infections, and allowing for sexual reproduction in pathogenic Candida species. Candida tropicalis, which is both an emerging human fungal pathogen and an environmental fungus, can switch between two heritable cell types termed white and opaque. In this study, we report the discovery of a novel phenotype in C. tropicalis, named the gray phenotype. Similar to Candida albicans and Candida dubliniensis, white, gray, and opaque cell types of C. tropicalis also form a tristable switching system, where gray cells are relatively small and elongated. In C. tropicalis, gray cells exhibit intermediate levels of mating competency and virulence in a mouse systemic infection model compared to the white and opaque cell types, express a set of cell type-enriched genes, and exhibit both common and species-specific biological features. The key regulators of white-opaque transitions, Wor1 and Efg1, are not required for the gray phenotype. A comparative study of the gray phenotypes in C. tropicalis, C. albicans, and C. dubliniensis provides clues to explain the species differences in terms of virulence, ecological niches, and prevalence among these three species.

2017-01-30 | GSE81514 | GEO

White Cells Facilitate Opposite- and Same-Sex Mating of Opaque Cells in Candida albicans

Project description:Modes of sexual reproduction in eukaryotic organisms are highly diversified. The human fungal pathogen Candida albicans undergoes a phenotypic switch from the white to the opaque phase in order to become mating-competent. In this study, we report that functionally and morphologically differentiated white and opaque cells show a coordinating behavior in the process of mating. Although white cells are mating-incompetent, they are induced to produce sexual pheromones when treated with opposite pheromones or interacted with opaque cells of an opposite mating type. In a co-culture system, pheromones released by white cells induce opaque cells to form mating projections and thus facilitate both opposite- and same-sex mating of opaque cells. Deletion of genes encoding the pheromone precursor proteins and inactivation of the pheromone response signaling pathway (Ste2-MAPK-Cph1) impair the promoting role of white cells (MTLa) in sexual mating of opaque cells. White and opaque cells communicate via a paracrine pheromone signaling and thus create an environment conducive to sexual mating. This coordination behavior of the two different cell types may be a trade-off strategy between sexual and asexual lifestyles in C. albicans. total RNA profiles of white cell treated with pheromone

2014-10-23 | E-GEOD-56039 | biostudies-arrayexpress

White Cells Facilitate Opposite- and Same-Sex Mating of Opaque Cells in Candida albicans

2014-10-23 | GSE56039 | GEO

Candida tropicalis

Project description:Discovery of a phenotypic switch regulating sexual mating in the opportunistic fungal pathogen Candida tropicalis

| PRJNA173866 | ENA

Passage through the mammalian gut triggers a phenotypic switch required for Candida albicans commensalism

Project description:Among ~5,000,000 fungal species on Earth, Candida albicans is exceptional in its lifelong association with humans, where it exists either as a benign component of the gastrointestinal microbiome or as an invasive pathogen. Although it is generally assumed that invasiveness results from a breakdown of host immunity , it is also possible that specific fungal programs control the transition between these divergent lifestyles. Here, we report that exposure of C. albicans to the mammalian gut triggers a developmental switch, driven by the Wor1 transcription factor, to a commensal cell type. Wor1 has been thought to occur only in unique genetic backgrounds, but we show that WOR1 expression is triggered when wild-type cells are propagated in a murine gastrointestinal infection model. Similar to Wor1’s role in a white-opaque switch for mating, WOR1 overexpression within the host induces a novel switch affecting cell and colony morphology and conferring commensal fitness. However, these hyperfit GUT (Gastrointestinally-IndUced Transition) cells lack the functional hallmarks of opaque cells, which they resemble morphologically, whereas bona fide opaque cells are defective for commensalism. Instead, the GUT cell transcriptome is optimized for the environment of the distal mammalian digestive tract. The GUT cell type switch illuminates how a single organism can utilize distinct genetic programs to transition between commensalism and invasive tissue pathogenesis

2013-07-28 | GSE43972 | GEO

Passage through the mammalian gut triggers a phenotypic switch required for Candida albicans commensalism

2013-07-28 | E-GEOD-43972 | biostudies-arrayexpress

A velvet transcription factor specifically activates mating through a novel surface protein in the human fungal pathogen Cryptococcus deneoformans

Project description:Sexual reproduction facilitates infection by the production of both a lineage advantage and infectious sexual spores in the ubiquitous human fungal pathogen Cryptococcus deneoformans. However, the regulatory determinants specific for initiating mating remain poorly understood. Here, we identified a velvet family regulator, Cva1, that strongly promotes sexual reproduction in C. deneoformans. This regulation was determined to be specific, based on a comprehensive phenotypic analysis of cva1 under 25 distinct in vitro and in vivo growth conditions. We further revealed that Cva1 plays a critical role in the initiation of early mating events, especially sexual cell-cell fusion, but is not important for the late sexual development stages or meiosis. Thus, Cva1 specifically contributes to mating activation. Importantly, a novel mating-responsive surface protein, Cfs1, serves as the key target of Cva1 during mating, since its absence nearly blocks cell-cell fusion in C. deneoformans and its sister species C. neoformans. Together, our findings provide insight into how C. deneoformans ensures regulatory specificity of mating.

2022-02-10 | GSE196267 | GEO

Glucose depletion enables Candida albicans mating independent of the epigenetic white-opaque switch

Project description:The human fungal pathogen Candida albicans can switch stochastically and heritably between a “white” phase and an “opaque” phase. Opaque cells are the mating-competent form of the species whereas white cells are essentially “sterile”. Here, we report that glucose depletion, a common nutrient stress, enables C. albicans white cells to undergo efficient sexual mating. The relative expression levels of pheromone-sensing and mating-associated genes (including STE2/3, MFA1, MFalpha1, FIG1, FUS1, and CEK1/2) were increased under glucose depletion conditions, while expression of mating repressors TEC1 and DIG1 was decreased. We show that Cph1 and Tec1, factors that act downstream of the pheromone MAPK pathway, play opposite roles in regulating white cell mating as TEC1 deletion or CPH1 overexpression promoted white cell mating. Moreover, inactivation of the Cph1 repressor Dig1 increased white cell mating ~4,000 fold in glucose-depleted medium relative to that in the presence of glucose. These findings reveal that the white-to-opaque epigenetic switch may not be a prerequisite for sexual mating in C. albicans in nature. Given parallels between C. albicans white cell mating to that of other yeast species, this mechanism of mating could represent a more ancient strategy of sexual reproduction in C. albicans.

2023-03-03 | PXD040559 | iProX

Drosophila female reproductive glands contribute to mating plug composition and the timing of sperm ejection

Project description:Reproductive traits that influence female remating and competitive fertilization rapidly evolve in response to sexual selection and sexual conflict. One such trait, observed across diverse animal taxa, is the formation of a structural plug inside the female reproductive tract, either during or shortly after mating. In Drosophila melanogaster, male seminal fluid forms a mating plug inside the female bursa, which has been demonstrated to influence sperm entry into storage and latency of female remating. Processing of the plug, including its eventual ejection from the female's reproductive tract, influences the competitive fertilization success of her mates and is mediated by female × male genotypic interactions. However, female contributions to plug formation and processing have received limited attention. Using developmental mutants that lack glandular female reproductive tract tissues, we reveal that these glandular tissues are essential for the mating plug to be ejected. We further use proteomics to demonstrate that female glandular proteins, and especially proteolytic enzymes, contribute to mating plug composition and that the absence of glands has a widespread impact of plug formation and composition. Together, these phenotypic and molecular data resolve molecular mechanisms of important postmating, intersexual interactions and cryptic female choice.

2022-01-25 | PXD028524 | Pride

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