Life Cycle of<i>Cryptococcus neoformans</i>

Zhao, Youbao; Lin, Jianfeng; Fan, Yumeng; Lin, Xiaorong

doi:10.1146/annurev-micro-020518-120210

Cited by 84 publications

(102 citation statements)

References 185 publications

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“…However, diploid and aneuploid strains can also be found in both clinical and environmental sources. It can reproduce both asexually via budding and sexually via mating (Zhao et al, 2019). During asexual reproduction, both the nuclear and mitochondrial genomes are faithfully transmitted from the parental cells to offspring.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial Genome Polymorphisms in the Human Pathogenic Fungus Cryptococcus neoformans

Wang

2020

Front. Microbiol.

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The Cryptococcus complex consists of at least seven evolutionary divergent lineages and causes ∼200,000 fatal human infections each year worldwide. The dominant lineage is Cryptococcus neoformans which consists of three haploid clades VNI, VNII, and VNB, their haploid hybrids, and various diploids derived from intra-and interclade mating events. In this study, we analyzed the mitogenomes of 184 strains of C. neoformans. Our analyses revealed that all 184 mitogenomes contained the same 15 protein-coding genes in the same gene order. However, their mitogenome sizes varied between 24,740 and 31,327 bp, primarily due to differences in the number and size of mitochondrial introns. Twelve nucleotide sites within five mitochondrial genes were found to contain introns in at least one of the 184 strains, ranging from 2 to 7 introns within each mitogenome. The concatenated mitochondrial exon sequences of the 15 protein-coding genes and two rRNA genes showed that VNI, VNII, and VNB strains were separated into distinct clades or sub-clades, largely consistent with results based on nuclear genome SNPs. However, several novel findings were observed. First, one strain of the VNB clade contained mitogenome exon sequences identical to the main VNI mitogenome type but was distant to other VNB mitogenomes. Second, hybrids among clades VNI, VNII, and VNB identified based on their nuclear genome SNPs contained mitogenomes from different clades, with evidence of their mitogenomes inherited from either the MATa or the MATα parents. Third, the eight diploid VNB (C. neoformans) × VNIV (C. deneoformans) hybrids contained recombinant mitogenomes. Fourth, analyses of intron distribution and the paired exonintron phylogenies for each of the 12 exon-intron pairs suggested frequent gains and losses of mitochondrial introns during the evolution of C. neoformans. The combined mitogenome exon-based phylogeny and intron distributions suggested that clades VNI, VNII and VNB could be further divided into sub-clades. Together, our results revealed a dynamic evolution of mitochondrial genomes in this important human fungal pathogen.

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Section: Introductionmentioning

confidence: 99%

Mitochondrial Genome Polymorphisms in the Human Pathogenic Fungus Cryptococcus neoformans

Wang

2020

Front. Microbiol.

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“…This may suggest that C. neoformans needs unisexual reproduction for unique advantages other than syngamy-dependent genetic variance in sexual offspring. Indeed, a considerable dispersal benefit has been proven to be related to unisexual air-borne spores and filaments [47], which also help prevent against engulfment by amoeboid predator [22]. In addition, unisexual reproduction can produce ploidy variance among progenies that contributes to de novo genotypic and phenotypic plasticity [48].…”

Section: Discussionmentioning

confidence: 99%

“…This fungus is a prevalent human fungal pathogen causing more than 200,000 new human infections annually [5], and sex is hypothesized to contribute to its infections through meiosis-created lineage advantages [6–10] and infectious meiospores [11–17]. C. neoformans has two mating types (α and a ) and can undergo two sexual cycles, α- a bisexual and unisexual reproduction (also named haploid fruiting), which involves only a single mating type (mainly α) [18–22]. Due to an extreme bias of α in populations (>99%) in nature that may result in infrequent bisexual mating, α unisexual reproduction is considered to be the major sexual form in C. neoformans [22–24].…”

Section: Introductionmentioning

confidence: 99%

“…C. neoformans has two mating types (α and a ) and can undergo two sexual cycles, α- a bisexual and unisexual reproduction (also named haploid fruiting), which involves only a single mating type (mainly α) [18–22]. Due to an extreme bias of α in populations (>99%) in nature that may result in infrequent bisexual mating, α unisexual reproduction is considered to be the major sexual form in C. neoformans [22–24]. Cryptococcal unisexual reproduction can be differentiated from bisexual reproduction by molecular and morphological events [21, 25].…”

Section: Introductionmentioning

confidence: 99%

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Elucidation of the determinant for orchestration of solo unisexual cycle in an important human fungal pathogen

Liu

Chen

et al. 2019

Preprint

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38In fungi, the sex-determination program universally directs sexual development and 39 syngamy (the fusion of gametes) that underlies pre-meiotic diploidization. However, 40 the contribution of sex-determination to syngamy-independent sexual cycle, which 41 requires autopolyploidization as an alternative approach to elevate ploidy before 42 meiosis, remains unclear in fungi and other eukaryotes. The human fungal pathogen 43 Cryptococcus neoformans, as a model organism for studying fungal sexual 44 reproduction, can undergo syngamy-dependent bisexual and syngamy-independent 45 solo unisexual reproduction, in which endoreplication is considered to enable pre-46 meiotic self-diploidization. Here, by characterizing a mutant lacking all the core sex-47 determination factors, we show that sex-determination plays a central role in bisexual 48 syngamy but is not strictly required for unisexual development and self-diploidization. 49 This implies an unknown circuit, rather than the sex-determination program, for 50 specifically coordinating Cryptococcus unisexual cycle. We reveal that syngamy and 51 self-diploidization are both governed by the Qsp1-directed paracrine system via two 52 regulatory branches, Vea2 and Cqs2. Vea2 directs bisexual syngamy through the sex-53 determination program; conversely, Cqs2 is dispensable for bisexual syngamy but 54 activates unisexual endoreplication. Through functional profiling of 41 transcription 55 factors documented to regulate Cryptococcus sexual development, we reveal that only 56 Cqs2 can drive and integrate all unisexual phases and ensure the production of 57 meiospore progenies. Furthermore, ChIP-seq analysis together with genetic evaluation 58 indicate that Cqs2 induces unisexual self-diploidization through its direct control of 59 PUM1, whose expression is sufficient to drive autopolyploidization. Therefore, Cqs2 60 serves as the critical determinant that orchestrates Cryptococcus multistage unisexual 61 cycle that does not strictly require the sexual-determination program. 62 63 64 65 66 67 68 69 70 71 Introduction 72A sex-determination system is used for the development of sexual characteristics in 73 evolutionally diverse eukaryotes, including fungi [1]. In fungi, the sex-determination 74 system universally directs syngamy (the fusion of gametes to enable pre-meiotic 75 diploidization) and sexual differentiation events during either heterothallic or 76 homothallic mating [2, 3]. However, syngamy does not always underlie sexual 77 development and the two processes can be unconnected in many eukaryotes [4]; the 78 contribution of sex-determination to the fitness related to syngamy-independent solo 79 sexual cycle has yet to be investigated in fungi or other eukaryotes. Cryptococcus 80 neoformans is a model organism for studying fungal sexual reproduction. This fungus 81 is a prevalent human fungal pathogen causing more than 200,000 new human infections 82 annually [5], and sex is hypothesized to contribute to its infections through meiosis-83 created lineage adv...

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“…At the onset of meiosis, the tip of an aerial hypha enlarges to form a basidium within which the two parental nuclei fuse and meiosis occurs to produce four recombinant, haploid nuclei. The daughter nuclei undergo repeated mitotic divisions with individual nuclei packaged into individual basidiospores that bud off from the basidium, consequently forming four chains of basidiospores [26][27][28]. Sexual mating in Cryptococcus is normally restricted to cells of opposite mating types.…”

Section: Sexual Cycle Of Cryptococcusmentioning

confidence: 99%

Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

Samarasinghe

You

Jenkinson

et al. 2020

Genes

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Hybridization is increasingly recognized as an important force impacting adaptation and evolution in many lineages of fungi. During hybridization, divergent genomes and alleles are brought together into the same cell, potentiating adaptation by increasing genomic plasticity. Here, we review hybridization in fungi by focusing on two fungal pathogens of animals. Hybridization is common between the basidiomycete yeast species Cryptococcus neoformans × Cryptococcus deneoformans, and hybrid genotypes are frequently found in both environmental and clinical settings. The two species show 10–15% nucleotide divergence at the genome level, and their hybrids are highly heterozygous. Though largely sterile and unable to mate, these hybrids can propagate asexually and generate diverse genotypes by nondisjunction, aberrant meiosis, mitotic recombination, and gene conversion. Under stress conditions, the rate of such genetic changes can increase, leading to rapid adaptation. Conversely, in hybrids formed between lineages of the chytridiomycete frog pathogen Batrachochytrium dendrobatidis (Bd), the parental genotypes are considerably less diverged (0.2% divergent). Bd hybrids are formed from crosses between lineages that rarely undergo sex. A common theme in both species is that hybrids show genome plasticity via aneuploidy or loss of heterozygosity and leverage these mechanisms as a rapid way to generate genotypic/phenotypic diversity. Some hybrids show greater fitness and survival in both virulence and virulence-associated phenotypes than parental lineages under certain conditions. These studies showcase how experimentation in model species such as Cryptococcus can be a powerful tool in elucidating the genotypic and phenotypic consequences of hybridization.

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Life Cycle ofCryptococcus neoformans

Cited by 84 publications

References 185 publications

Mitochondrial Genome Polymorphisms in the Human Pathogenic Fungus Cryptococcus neoformans

Mitochondrial Genome Polymorphisms in the Human Pathogenic Fungus Cryptococcus neoformans

Elucidation of the determinant for orchestration of solo unisexual cycle in an important human fungal pathogen

Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

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