Hybrids and hybridization in the Cryptococcus neoformans and Cryptococcus gattii species complexes

Samarasinghe, Himeshi; Xu, Jianping

doi:10.1016/j.meegid.2018.10.011

Cited by 44 publications

(29 citation statements)

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“…The human pathogenic Cryptococcus species complex contains at least seven evolutionary divergent lineages and their hybrids (Hagen et al, 2015, Hagen et al, 2017Kwon-Chung et al, 2017;Samarasinghe and Xu, 2018). Together, they are responsible for over 200,000 deaths per year globally (Rajasingham et al, 2017).…”

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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“…The increasing prevalence of AD hybrids among clinical samples necessitates a better understanding of the hybridisation process between Cryptococcus species and the potential for increased virulence in resulting hybrids . Transgressive segregation in virulence and virulence‐associated phenotypes has been observed in previous interspecific crosses of Cryptococcus .…”

Section: Discussionmentioning

confidence: 99%

“…Haploid C neoformans and C deneoformans strains can hybridise with each other in nature to produce diploid/aneuploid hybrid strains, commonly referred to as AD hybrids . Initially discovered in the late 1970s, AD hybrids have since been recovered from both environmental and clinical samples with a high prevalence in Mediterranean Europe, where up to 30% of all cryptococcal infections are caused by hybrid strains . AD hybrids can also be generated under laboratory conditions by mating strains of the two species with each other, albeit with low spore germination rates of ~5% to 20% .…”

Section: Introductionmentioning

confidence: 99%

“…4,5 Initially discovered in the late 1970s, AD hybrids have since been recovered from both environmental and clinical samples with a high prevalence in Mediterranean Europe, where up to 30% of all cryptococcal infections are caused by hybrid strains. [6][7][8][9][10] AD hybrids can also be generated under laboratory conditions by mating strains of the two species with each other, albeit with low spore germination rates of ~5% to 20%. 5,11,12 Hybrid spores that do germinate often contain an abnormal number of chromosomes, consistent with impaired meiosis and non-disjunction of parental chromosomes during hybridisation.…”

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Patterns of allele distribution in a hybrid population of the Cryptococcus neoformans species complex

Samarasinghe

Vogan

Pum

et al. 2019

Mycoses

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Summary Background The sister yeast species Cryptococcus neoformans (serotype A) and Cryptococcus deneoformans (serotype D) are causative agents of deadly cryptococcosis and fungal meningoencephalitis. These haploid yeasts can hybridise in nature, giving rise to AD hybrids that are predominantly diploid or aneuploid. Despite their increasing prevalence in clinical settings, much remains unknown about the allelic distribution patterns in AD hybrid strains. Objectives This study aims to characterise allele distributions in AD hybrids derived from the same basidium as well as from multiple basidia in a laboratory‐derived C neoformans × C deneoformans hybrid cross. Methods We dissected a total of 1625 basidiospores from 31 basidia. The 297 basidiospores that successfully germinated were genotyped by molecular characterisation of 33 markers using PCR‐RFLP, with at least two markers on each of the 14 chromosomes in the genome. Results Of the 297 strains, 294 contained at least one heterozygous locus, with a mean heterozygosity of ~30% per strain. Most hybrid genomes and chromosomes displayed significantly distorted allele distributions, with offspring originating from the same basidium tended to have alleles at different loci from the same parent. More basidia were skewed in favour of C deneoformans alleles, the mitochondria‐donor parent, than the C neoformans alleles. Conclusions The divergence between C neoformans and C deneoformans genomes has likely created co‐adapted allelic combinations, with their co‐segregation in hybrid offspring imparting a significant fitness benefit. However, the diversity of genotypes recovered here in a single hybridisation event indicates the enormous capacity of AD hybrids for adaptation and diversification.

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“…Since their initial discovery in 1977, their prevalence has been steadily increasing, with AD hybrids currently causing up to 40% of all cryptococcal infections in Europe [47][48][49][50]. They have been recovered from clinical and environmental sources in many countries, across most continents [51]. AD hybrids are typically diploid or aneuploid and experience frequent loss of heterozygosity during vegetative growth [52][53][54].…”

Section: Hybrids In the Cryptococcus Species Complexmentioning

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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Hybrids and hybridization in the Cryptococcus neoformans and Cryptococcus gattii species complexes

Cited by 44 publications

References 128 publications

Mitochondrial Genome Polymorphisms in the Human Pathogenic Fungus Cryptococcus neoformans

Mitochondrial Genome Polymorphisms in the Human Pathogenic Fungus Cryptococcus neoformans

Patterns of allele distribution in a hybrid population of the Cryptococcus neoformans species complex

Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

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