Horizontal Transfer of Entire Chromosomes in Fungal Pathogens

The remarkable success of many bacterial pathogens is linked to their ability to exchange genetic material horizontally (laterally) through highly regulated mechanisms such as conjugation. In fungal eukaryotes, horizontal transfer of entire chromosomes has been reported, typically involving accessory chromosomes, yet it remains unclear whether and how
these transfers are regulated.
We show that a single accessory chromosome is transferred frequently and with striking specificity between different species of the fungal genus Metarhizium both in vitro and in the field. In co-inoculation experiments involving a donor strain carrying the accessory chromosome and an acceptor strain lacking it, up to 20% of resulting asexual spores of the acceptor strain carried the horizontally transferred chromosome. Transfers occurred between all four Metarhizium species tested, which diverged up to 15 MYA, and always involved only this one accessory chromosome. Furthermore, in Metarhizium isolates
collected worldwide, we identified a large number of accessory chromosomes, most of which show strong signatures of past horizontal transfer. Remarkably, these mobile chromosomes share a core gene set enriched for predicted DNA-binding and chromatin-conformation functions, raising the tantalizing possibility that the mobile chromosome itself encodes
factors required for its own horizontal mobility.
The high frequency, specificity, global distribution, and shared gene content of these horizontally transferred chromosomes point to a widespread, regulated mechanism of chromosome mobility in asexual fungi - potentially analogous to conjugative plasmids in bacteria.