The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogenCandida orthopsilosis

Abstract

<jats:title>Abstract</jats:title><jats:p>Interspecific hybridization can drive evolutionary adaptation to novel environments. The <jats:italic>Saccharomycotina</jats:italic> clade of budding yeasts includes many hybrid lineages, and hybridization has been proposed as a source for new pathogenic species. <jats:italic>Candida orthopsilosis</jats:italic> is an emerging opportunistic pathogen for which most clinical isolates are hybrids, each derived from one of at least four independent crosses between the same two parental lineages. To gain insight on the transcriptomic aftermath of hybridization in these pathogens, we analyzed allele-specific gene expression in two independently formed hybrid strains, and in a homozygous strain representative of one parental lineage. Our results show that the effect of hybridization on overall gene expression is rather limited, affecting ~4% of the studied genes. However, we identified a larger effect in terms of imbalanced allelic expression, affecting ~9.5% of the heterozygous genes in the hybrids. Some of these altered genes have functions related to pathogenicity, including zinc transport and superoxide dismutase activities. Additionally, the number of shared genes with imbalanced expression in the two independently formed hybrids was higher than random expectation, suggesting selective retention. While it remains unclear whether the observed imbalanced genes play a role in virulence, our results suggest that differences in allele-specific expression may add an additional layer of phenotypic plasticity to traits related to virulence in <jats:italic>C. orthopsilosis</jats:italic> hybrids.</jats:p><jats:sec><jats:title>Importance</jats:title><jats:p>How new pathogens emerge is an important question that remains largely unanswered. Some emerging yeast pathogens are hybrids originated through the crossing of two different species, but how hybridization contributes to a higher virulence is unclear. Here we show that hybrids selectively retain gene regulation plasticity inherited from the two parents, and that this plasticity affects genes involved in virulence.</jats:p></jats:sec>

Editorial: Genomic insights on fungal hybrids

“…Contrary to expectations from this hypothesis, the Drouin et al study shows that transposable elements are generally not differentially expressed in hybrids, even when exposed to stress conditions. This result adds to recent findings on the overall maintenance of gene expression patterns in yeast hybrids (Hovhannisyan et al, 2020a;Hovhannisyan et al, 2020b), and suggests that the genomic shock hypothesis, which was proposed based on observations of plant hybrids, may not hold for yeast hybrids. Another article from Bendixsen et al focuses on genomic variation following hybridization by analyzing genomic data from over 200 naturally occurring hybrids between different species of the genus Saccharomyces.…”

“…Compared to their parents, hybrids sometimes show higher adaptive capacities towards specific niches, thereby contributing to diversification (Abbott et al, 2013). Fungal hybrids have been neglected by formal studies for a long time due to the inherent challenges of the microbial species concept and the difficulty of identifying hybrids based on morphological characters (Gabaldoń, 2020a;Boekhout et al, 2021). Although the first fungal hybrids were identified in Saccharomyces, thanks to careful dissection of metabolic properties (Morales and Dujon, 2012) and emerging genome sequencing technologies (Hittinger, 2013), it was the spread of these sequencing technologies that revealed the true pervasiveness of hybrids across the fungal tree of life (Naranjo-Ortiz and Gabaldoń, 2020; Gabaldoń, 2020b).…”