Abstract
Interspecific hybridization can drive evolutionary adaptation to novel environments. The Saccharomycotina clade of budding yeasts includes many hybrid lineages, and hybridization has been proposed as a source for new pathogenic species. Candida orthopsilosis 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 into 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 genes studied. However, we identified a larger effect in terms of imbalanced allelic expression, affecting ∼9.5% of the heterozygous genes in the hybrids. This effect was larger in the hybrid with more extensive loss of heterozygosity, which may indicate a tendency to avoid loss of heterozygosity in these genes. Consistently, the number of shared genes with allele-specific expression in the two independently formed hybrids was higher than random expectation, suggesting selective retention. Some of the imbalanced genes have functions related to pathogenicity, including zinc transport and superoxide dismutase activities. 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 C. orthopsilosis hybrids.IMPORTANCE 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 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.
Highlights
Interspecific hybridization can drive evolutionary adaptation to novel environments
The fact that some parental species of hybrid fungal pathogens are never or rarely identified among clinical isolates suggests that some human pathogens have arisen from nonpathogenic parental organisms [5, 13], or that the parental lineages have been outcompeted by their more-adapted pathogenic hybrid descendants [17,18,19]
The two analyzed hybrid strains belong to two independently formed hybrid clades resulting from the mating of the same two parental lineages: strain MCO456 belongs to hybrid clade 1, which underwent extensive loss of heterozygosis (LOH), whereas strain CP124 belongs to clade 4, which has limited LOH (Fig. 1)
Summary
Interspecific hybridization can drive evolutionary adaptation to novel environments. The Saccharomycotina clade of budding yeasts includes many hybrid lineages, and hybridization has been proposed as a source for new pathogenic species. To gain insight into 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. Some of the imbalanced genes have functions related to pathogenicity, including zinc transport and superoxide dismutase activities 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 C. orthopsilosis hybrids. Hybridization results in a state often referred as a “genomic shock” [20], in which two diverged genomes which have evolved independently for a certain time are sharing the same cellular environment This coexistence can lead to alterations at several levels, including the genome [21], transcriptome [22], or proteome [23], among others [24]. Our understanding of the impact of hybridization at the transcriptomic level remains poorly characterized, with few studies performed on industrial or plant saprophyte hybrids [22, 27,28,29,30]
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