Metabolic Conservation and Diversification of Metarhizium Species Correlate with Fungal Host-Specificity

Abstract

The ascomycete genus Metarhizium contains several species of insect pathogenic fungi ranging from specialists with narrow host ranges to generalists that can infect diverse invertebrates. Genetic and metabolic conservations and diversifications of Metarhizium species are not well understood. In this study, using the genome information of seven Metarhizium species, we performed a comparative analysis of gene clusters involved in secondary metabolisms (SMs) in these species. The results revealed that the generalist species contain more SM gene clusters than the specialists, and that both conserved and divergent evolutions may have occurred in SM genes during fungal speciation. In particular, the loss/gain events, as well as gene mutagenesis, are evident for the gene cluster responsible for the biosynthesis of non-ribosomal cyclopeptide destruxins. The presence of conserved SM gene clusters in Metarhizium and other divergently evolved insect pathogenic fungi implies their link to fungal entomopathogenicity. Mass spectrometry based metabolomic analyses were also conducted to investigate the chemical diversities of seven Metarhizium species. Consistent with the evolutionary relationships of SM genes among the seven species, significant differences are observed in fungal metabolic profiles, whether the same or different metabolites are produced in different species. Clustering analysis based on the metabolome data revealed that Metarhizium species could be grouped based on their association to fungal host specificity. Our metabolomics-based methods also facilitate the identification of bioactive metabolites that have not been reported previously in Metarhizium. The results of this study will benefit future investigations of the chemical biology of insect-fungal interactions.

Tryptamine accumulation caused by deletion of MrMao-1 in Metarhizium genome significantly enhances insecticidal virulence

“…The smaller number suggests that MAC may rely on simple metabolites to improve its virulence against insects owing to the biosynthesis cost. MAC can produce other cytotoxic antibiotic metabolites [11], however the pathogenesis of such metabolites in contributing to the virulence of MAC still needs to be investigated.…”

“…Further comparative genomic analysis showed that MAC presents less virulence genes, including chitinase, protease, and secondary metabolic gene clusters [7]. Interestingly, MAC lacks the genes for the biosynthesis of the virulence factor destruxin compared with MAA [7,11]. In fact, destruxin allows MAA to inhibit the system activity of prophenoloxidase and the production of bactericidal peptides of hosts, suppressing the hosts' immune defense and increasing the opportunistic infection of microbes in host insects [12,13].…”

“…Metarhizium species are fungal insect pathogens that can synthesize secondary metabolites of insecticidal and antibacterial compounds [11,14]. The metabolite destruxin is considered the most important insecticidal factor of the Metarhizium species.…”

Orthologous peramine and pyrrolopyrazine‐producing biosynthetic gene clusters in Metarhizium rileyi, Metarhizium majus and Cladonia grayi

“…However, it has also been demonstrated that DTX are dispensable for pathogenicity against some hosts (Donzelli et al ., ), while other Metarhizium spp. lack the DTX cluster entirely (Xu et al ., ). This suggests that other as‐yet unidentified insecticidal SMs may play analogous roles in these species.…”

“…. Furthermore, Xu et al (2016) recently demonstrated an association between evolution of modern generalist Metarhizium spp. and acquisition of this DTX cluster, suggesting a role for DTX in adaptation to a wider host-range.…”