Horizontal gene transfer allowed the emergence of broad host range entomopathogens

Abstract

The emergence of new pathogenic fungi has profoundly impacted global biota, but the underlying mechanisms behind host shifts remain largely unknown. The endophytic insect pathogen Metarhizium robertsii evolved from fungi that were plant associates, and entomopathogenicity is a more recently acquired adaptation. Here we report that the broad host-range entomopathogen M. robertsii has 18 genes that are derived via horizontal gene transfer (HGT). The necessity of degrading insect cuticle served as a major selective pressure to retain these genes, as 12 are up-regulated during penetration; 6 were confirmed to have a role in penetration, and their collective actions are indispensable for infection. Two lipid-carrier genes are involved in utilizing epicuticular lipids, and a third (MrNPC2a) facilitates hemocoel colonization. Three proteases degraded the procuticular protein matrix, which facilitated up-regulation of other cuticle-degrading enzymes. The three lipid carriers and one of the proteases are present in all analyzed Metarhizium species and are essential for entomopathogenicity. Acquisition of another protease (MAA_01413) in an ancestor of broad host-range lineages contributed to their host-range expansion, as heterologous expression in the locust specialist Metarhizium acridum enabled it to kill caterpillars. Our work reveals that HGT was a key mechanism in the emergence of entomopathogenicity in Metarhizium from a plant-associated ancestor and in subsequent host-range expansion by some Metarhizium lineages.

A M35 family metalloprotease is required for fungal virulence against insects by inactivating host prophenoloxidases and beyond

“…Chitin-binding LysM effectors can be transcribed by B. bassiana to protect fungal cell walls and to suppress insect immunities [36]. A sterol carrier protein horizontally acquired from insect hosts in Metarhizium can facilitate the dispersal of fungal cells in the host body cavity [56,57]. It has also been found that small molecules such as destruxins, cyclosporins, and oosporein as well as the small RNAs produced by entomopathogens can inhibit insect cellular and/or humoral immune responses upon fungal infections [38,[58][59][60].…”

Population-Specific Selection on Standing Variation Generated by Lateral Gene Transfers in a Grass

“…Evidence of eukaryote-to-eukaryote lateral gene transfer (LGT) has accumulated in recent years [1][2][3][4][5][6][7][8][9][10][11][12][13][14], but the selective pressures governing the evolutionary fate of these genes within recipient species remain largely unexplored [15,16]. Among nonparasitic plants, successful LGT has been reported between different grass species [5,8,11,[16][17][18][19].…”

Revisiting Metarhizium and the description of new species from Thailand

“…2020 ). Recent genome sequencing projects on Metarhizium tried to focus on host associations ( Hu et al., 2014 , Zhang et al., 2019 ) claiming some species are more host-specific than others. Correct identification of the species and its host-range, thus using the right species for biological control of agricultural pests is paramount to a successful biocontrol strategy.…”