Frequent horizontal chromosome transfer between asexual fungal insect pathogens

Abstract

Entire chromosomes are typically only transmitted vertically from one generation to the next. The horizontal transfer of such chromosomes has long been considered improbable, yet gained recent support in several pathogenic fungi where it may affect the fitness or host specificity. To date, it is unknown how these transfers occur, how common they are and whether they can occur between different species. In this study, we show multiple independent instances of horizontal transfers of the same accessory chromosome between two distinct strains of the asexual entomopathogenic fungus Metarhizium robertsii during experimental co-infection of its insect host, the Argentine ant. Notably, only the one chromosome - but no other - was transferred from the donor to the recipient strain. The recipient strain, now harboring the accessory chromosome, exhibited a competitive advantage under certain host conditions. By phylogenetic analysis we further demonstrate that the same accessory chromosome was horizontally transferred in a natural environment between M. robertsii and another congeneric insect pathogen, M. guizhouense. Hence horizontal chromosome transfer is not limited to the observed frequent events within species during experimental infections but also occurs naturally across species. The transferred accessory chromosome contains genes that might be involved in its preferential horizontal transfer, encoding putative histones and histone-modifying enzymes, but also putative virulence factors that may support its establishment. Our study reveals that both intra- and interspecies horizontal transfer of entire chromosomes is more frequent than previously assumed, likely representing a not uncommon mechanism for gene exchange.

Multiple horizontal mini-chromosome transfers drive genome evolution of clonal blast fungus lineages

“…Parasexuality offers fungi an alternative route to enhancing genetic diversity, while maintaining relative genomic stability and avoiding the complexities of sexual reproduction, including pre-mating barriers like reproductive timing and post-mating issues such as hybrid incompatibilities (Roper et al 2011;Stukenbrock 2013). Recently, it was proposed that chromosome reassortment during parasexual recombination may not be entirely random (Habig et al 2023). Here, it was suggested that some mChr are preferentially transferred or tend to resist degradation compared to others, resembling the behavior of selfish genetic elements (Ahmad and Martins 2019).…”

“…This is exemplified in the case of Fusarium oxysporum, where the horizontal acquisition of a mChr in laboratory settings transformed a nonpathogenic strain into a virulent pathogen (Ma et al 2010). Similarly, in the insect pathogen Metarhizium robertsii, strains with a horizontally acquired mChr were more virulent compared to those without this mChr (Habig et al 2023). A notorious plant pathogenic fungus where asexually reproducing clonal lineages underlie crop pandemics, is the blast fungus Magnaporthe oryzae (Syn.…”