Infection of the entomopathogenic fungus Metarhizium rileyi suppresses cellular immunity and activates humoral antibacterial immunity of the host Spodoptera frugiperda.

Background: Metarhizium rileyi is an entomopathogenic fungus with promising potential for controlling agricultural pests, including Spodoptera frugiperda. Following penetration of the host through the cuticle, M. rileyi cells transform into in vivo blastospores or hyphal bodies, propagating within the hemocoel. However, the strategies and molecular mechanisms by which M. rileyi survives upon exposure to the powerful insect immune system remain unclear.

Results: We determined the pathogenicity of M. rileyi and found that either conidial immersion or blastospore injection significantly decreased S. frugiperda survival in a dose-dependent manner. Injection of M. rileyi blastospores decreased the number of S. frugiperda hemocytes and impaired host cellular reactions such as nodulation, encapsulation and phagocytosis. Blastospore injection led to increased antibacterial activity in plasma at 48 h post-injection (hpi). RNA-sequencing analyses identified a large number of antimicrobial peptide genes upregulated in the fat body of M. rileyi-infected larvae at 48 hpi, which may be attributable to the activation of Toll and IMD signaling pathway.

Conclusion: This study demonstrates that the compromised cellular immunity of the insect host is due to the marked decrease in hemocytes and impaired cellular cytoskeletons, which may facilitate early infection by M. rileyi. Late in the course of infection, the enhanced antibacterial activity of plasma, which may be in response to intestinal evading bacteria, cannot inhibit hyphal growth in hemolymph. Our data provide a comprehensive resource for exploring the molecular mechanism employed by M. rileyi to overcome S. frugiperda immunity. © 2022 Society of Chemical Industry.