On the evolution of variation in sexual reproduction through the prism of eukaryotic microbes

Yadav, Vikas; Sun, Sheng; Heitman, Joseph

doi:10.1073/pnas.2219120120

Cited by 11 publications

(5 citation statements)

References 173 publications

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“…Chromosomal rearrangements, including inversions, translocations, fusions, and fissions, underlie the extensive karyotypic variability seen across eukaryotes [26][27][28]. These sources of structural variation aid organisms in adapting to diverse environments [29,30], influence changes in mating systems [23,[31][32][33], drive the evolution of pathogenic traits [34][35][36], and play roles in speciation [37][38][39][40][41].…”

Section: Cryptococcus Amylolentus Cryptococcus Floricola Cryptococcus...mentioning

confidence: 99%

Comparative genomics ofCryptococcusandKwoniellareveals pathogenesis evolution and contrasting karyotype dynamics via intercentromeric recombination or chromosome fusion

Coelho,

David-Palma,

Shea

et al. 2023

Preprint

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A large-scale comparative genomic analysis was conducted for the global human fungal pathogens within theCryptococcusgenus, compared to non-pathogenicCryptococcusspecies, and related species from the sister genusKwoniella. Chromosome-level genome assemblies were generated for multiple species of both genera, resulting in a dataset encompassing virtually all of their known diversity. AlthoughCryptococcusandKwoniellahave comparable genome sizes (about 19.2 and 22.9 Mb) and similar gene content, hinting at pre-adaptive pathogenic potential, our analysis found evidence in pathogenicCryptococcusspecies of specific examples of gene gain (via horizontal gene transfer) and gene loss, which might represent evolutionary signatures of pathogenic development. Genome analysis also revealed a significant variation in chromosome number and structure between the two genera. By combining synteny analysis and experimental centromere validation, we found that mostCryptococcusspecies have 14 chromosomes, whereas mostKwoniellaspecies have fewer (11, 8, 5 or even as few as 3). Reduced chromosome number inKwoniellais associated with formation of giant chromosomes (up to 18 Mb) through repeated chromosome fusion events, each marked by a pericentric inversion and centromere loss. While similar chromosome inversion-fusion patterns were observed in allKwoniellaspecies with fewer than 14 chromosomes, no such pattern was detected inCryptococcus. Instead,Cryptococcusspecies with less than 14 chromosomes, underwent chromosome reductions primarily through rearrangements associated with the loss of repeat-rich centromeres. Additionally,Cryptococcusgenomes exhibited frequent interchromosomal translocations, including intercentromeric recombination facilitated by transposons shared between centromeres. Taken together, our findings advance our understanding of genomic changes possibly associated with pathogenicity inCryptococcusand provide a foundation to elucidate mechanisms of centromere loss and chromosome fusion driving distinct karyotypes in closely related fungal species, including prominent global human pathogens.

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Section: Cryptococcus Amylolentus Cryptococcus Floricola Cryptococcus...mentioning

confidence: 99%

Comparative genomics ofCryptococcusandKwoniellareveals pathogenesis evolution and contrasting karyotype dynamics via intercentromeric recombination or chromosome fusion

Coelho,

David-Palma,

Shea

et al. 2023

Preprint

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“…Some microbial eukaryotes can transition between vegetative cells and cysts or spores and some can undergo sexual reproduction with different cell types [18,19]. These different cell types could be considered as states but they are much less studied compared to those in multicellular eukaryotes [20]. Currently, very few microbial eukaryotes are available in the cultures and the ones that are, might not reflect the ecologically most important genera.…”

Section: Introductionmentioning

confidence: 99%

Towards high-throughput parallel imaging and single-cell transcriptomics of microbial eukaryotic plankton

Grujčić,

Saarenpää,

Sundh

et al. 2024

PLoS ONE

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Single-cell transcriptomics has the potential to provide novel insights into poorly studied microbial eukaryotes. Although several such technologies are available and benchmarked on mammalian cells, few have been tested on protists. Here, we applied a microarray single-cell sequencing (MASC-seq) technology, that generates microscope images of cells in parallel with capturing their transcriptomes, on three species representing important plankton groups with different cell structures; the ciliate Tetrahymena thermophila, the diatom Phaeodactylum tricornutum, and the dinoflagellate Heterocapsa sp. Both the cell fixation and permeabilization steps were adjusted. For the ciliate and dinoflagellate, the number of transcripts of microarray spots with single cells were significantly higher than for background spots, and the overall expression patterns were correlated with that of bulk RNA, while for the much smaller diatom cells, it was not possible to separate single-cell transcripts from background. The MASC-seq method holds promise for investigating "microbial dark matter”, although further optimizations are necessary to increase the signal-to-noise ratio.

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“…Chromosomal rearrangements, including inversions, translocations, fusions, and fissions, underlie the extensive karyotypic variability seen across eukaryotes [ 30 – 32 ]. These sources of structural variation aid organisms in adapting to diverse environments [ 33 , 34 ], influence changes in mating systems [ 27 , 35 – 37 ], drive the evolution of pathogenic traits [ 38 – 40 ], and play roles in speciation [ 41 – 45 ].…”

Section: Introductionmentioning

confidence: 99%

Comparative genomics of the closely related fungal genera Cryptococcus and Kwoniella reveals karyotype dynamics and suggests evolutionary mechanisms of pathogenesis

Coelho,

David-Palma,

Shea

et al. 2024

PLoS Biol

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In exploring the evolutionary trajectories of both pathogenesis and karyotype dynamics in fungi, we conducted a large-scale comparative genomic analysis spanning the Cryptococcus genus, encompassing both global human fungal pathogens and nonpathogenic species, and related species from the sister genus Kwoniella. Chromosome-level genome assemblies were generated for multiple species, covering virtually all known diversity within these genera. Although Cryptococcus and Kwoniella have comparable genome sizes (about 19.2 and 22.9 Mb) and similar gene content, hinting at preadaptive pathogenic potential, our analysis found evidence of gene gain (via horizontal gene transfer) and gene loss in pathogenic Cryptococcus species, which might represent evolutionary signatures of pathogenic development. Genome analysis also revealed a significant variation in chromosome number and structure between the 2 genera. By combining synteny analysis and experimental centromere validation, we found that most Cryptococcus species have 14 chromosomes, whereas most Kwoniella species have fewer (11, 8, 5, or even as few as 3). Reduced chromosome number in Kwoniella is associated with formation of giant chromosomes (up to 18 Mb) through repeated chromosome fusion events, each marked by a pericentric inversion and centromere loss. While similar chromosome inversion–fusion patterns were observed in all Kwoniella species with fewer than 14 chromosomes, no such pattern was detected in Cryptococcus. Instead, Cryptococcus species with less than 14 chromosomes showed reductions primarily through rearrangements associated with the loss of repeat-rich centromeres. Additionally, Cryptococcus genomes exhibited frequent interchromosomal translocations, including intercentromeric recombination facilitated by transposons shared between centromeres. Overall, our findings advance our understanding of genetic changes possibly associated with pathogenicity in Cryptococcus and provide a foundation to elucidate mechanisms of centromere loss and chromosome fusion driving distinct karyotypes in closely related fungal species, including prominent global human pathogens.

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On the evolution of variation in sexual reproduction through the prism of eukaryotic microbes

Cited by 11 publications

References 173 publications

Comparative genomics ofCryptococcusandKwoniellareveals pathogenesis evolution and contrasting karyotype dynamics via intercentromeric recombination or chromosome fusion

Comparative genomics ofCryptococcusandKwoniellareveals pathogenesis evolution and contrasting karyotype dynamics via intercentromeric recombination or chromosome fusion

Towards high-throughput parallel imaging and single-cell transcriptomics of microbial eukaryotic plankton

Comparative genomics of the closely related fungal genera Cryptococcus and Kwoniella reveals karyotype dynamics and suggests evolutionary mechanisms of pathogenesis

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