Adenylate cyclase orthologues in two filamentous entomopathogens contribute differentially to growth, conidiation, pathogenicity, and multistress responses

• Sole adenylate cyclase (AC) exists in B. bassiana (Bb) and M. robertstii (Mr).
• BbAC and MrAC disruptions caused severe growth defects on rich and minimal media.
• Two deletion mutants showed antagonistic conidiation changes during cultivation.
• Their virulence and multistress tolerances changed differentially or reversely.
• BbAC and MrAC contribute differentially to the biocontrol potential of two fungi.

Adenylate cyclase (AC) is a core element of cAMP signalling network. Here we show functional diversity and differentiation of Beauveria bassiana AC (BbAC) and Metarhizium robertsii AC (MrAC). Severe growth defects occurred in ΔBbAC and ΔMrAC grown on nutrition-rich SDAY and several minimal media but were largely alleviated by adding cAMP to SDAY. Conidial yield increased greatly in ΔBbAC but decreased in ΔMrAC. During colony growth, ΔBbAC was highly sensitive to oxidation, high osmolarity, cell wall perturbation, carbendazim fungicide, Mn2+, Zn2+, Fe3+, and EDTA but more tolerant to Cu2+ while ΔMrAC showed higher osmotolerance, decreased sensitivity to Fe3+, and null response to carbendazim or cell wall stress despite similar responses to oxidation and other metal ions. Conidial UV-B resistance decreased by 32 % in ΔBbAC and 22 % in ΔMrAC despite little change in their theromotolerance. Median lethal time (LT50) estimates of ΔBbAC and ΔMrAC against susceptible insects were 10.9 and 1.4 d longer than those from wild-type strains respectively. All the phenotypic changes were restored to wild-type levels by each gene complementation. Taken together, BbAC and MrAC regulated differentially conidiation, pathogenicity, and multistress responses in B. bassiana and M. robertsii, thereby making different contributions to their biocontrol potential.