Altered Immunity in Crowded Locust Reduced Fungal ( Metarhizium anisopliae) Pathogenesis

Abstract

The stress of living conditions, similar to infections, alters animal immunity. High population density is empirically considered to induce prophylactic immunity to reduce the infection risk, which was challenged by a model of low connectivity between infectious and susceptible individuals in crowded animals. The migratory locust, which exhibits polyphenism through gregarious and solitary phases in response to population density and displays different resistance to fungal biopesticide ( Metarhizium anisopliae), was used to observe the prophylactic immunity of crowded animals. We applied an RNA-sequencing assay to investigate differential expression in fat body samples of gregarious and solitary locusts before and after infection. Solitary locusts devoted at least twice the number of genes for combating M. anisopliae infection than gregarious locusts. The transcription of immune molecules such as pattern recognition proteins, protease inhibitors, and anti-oxidation proteins, was increased in prophylactic immunity of gregarious locusts. The differentially expressed transcripts reducing gregarious locust susceptibility to M. anisopliae were confirmed at the transcriptional and translational level. Further investigation revealed that locust GNBP3 was susceptible to proteolysis while GNBP1, induced by M. anisopliae infection, resisted proteolysis. Silencing of gnbp3 by RNAi significantly shortened the life span of gregarious locusts but not solitary locusts. By contrast, gnbp1 silencing did not affect the life span of both gregarious and solitary locusts after M. anisopliae infection. Thus, the GNBP3-dependent immune responses were involved in the phenotypic resistance of gregarious locusts to fungal infection, but were redundant in solitary locusts. Our results indicated that gregarious locusts prophylactically activated upstream modulators of immune cascades rather than downstream effectors, preferring to quarantine rather than eliminate pathogens to conserve energy meanwhile increasing the “distance” of infectious and target individuals. Our study has obvious implications for bio-pesticides management of crowded pests, and for understanding disease epidemics and adaptiveness of pathogens.

Author Summary

The wide application of fungal biopesticides for insect management has led to concerns over the development of biopesticide resistance. The migratory locust, a globally notorious agricultural pest, has density-dependent phase changes between solitary and gregarious states. The gregarious locusts displayed longer life spans than solitary locusts after biopesticide Metarhizium anisopliae infection. We analyzed prophylactic immunity of the locusts in phase change adaptation by transcriptome analysis. Gregarious locusts optimized immunity by investing more in molecules of upstream immune cascades including pattern recognition proteins, anti-oxidation proteins, protease inhibitors and serine protease. High levels of pattern recognition proteins guided deposition of immune products onto pathogens reducing growth, proliferation and transmission. This prophylactic immunity of gregarious locusts emphasized on quarenteening M. anisopliae pathogens in early infection, which decreased individuals' infection risk in a population and avoids disease epidemics. Pest outbreaks mostly occur in high population densities, thereby, diminishing entomopathogen biopesticide efficiency. Our results provide an insight to an organism's “enhanced” immunity induced by population densities and inspires new paradigms to understand biopesticide tolerance and disease epidemics in the future.