Microbiota modulates gut immunity and promotes baculovirus infection in Helicoverpa armigera

Abstract

Baculoviruses are natural enemies of agricultural and forest insect pests and play an important role in biological pest control. Oral infection by baculovirus in the insect midgut is necessary for establishing systemic infection and eventually killing the insect. Since the insect midgut continuously encounters microbiota, the gut microbiota could affect baculovirus infection. Here, we demonstrated that gut microbiota modulates immune responses and promotes baculovirus infection in the cotton bollworm, Helicoverpa armigera. After oral infection, numerous host immunity‐related genes including genes encoding Toll and immune deficiency (IMD) pathway components were upregulated in the midgut. Elimination of the gut microbiota significantly increased the resistance to viral infection in H. armigera. Quantitative real‐time reverse transcription polymerase chain reaction and proteomic analysis showed that downregulation of the antiviral factor prophenoloxidase (PPO) could be mediated by microbiota during infection. It implied that midgut microbiota diminishes the expression of PPO to facilitate viral infection in H. armigera. Our findings revealed that the microbiota plays an important role in modulating the resistance of H. armigera to baculovirus infection, providing new insights in applying biopesticide.

Topical Fungal Infection Induces Shifts in the Gut Microbiota Structure of Brown Planthopper, Nilaparvata lugens (Homoptera: Delphacidae)

“…For example, gut microbiota of the beet armyworm Spodoptera exigua could enhance baculovirus virulence by modulating gut immunity [ 16 ]. Similar effects were found for the cotton bollworm Helicoverpa armigera [ 17 ], the gypsy moth Lymantria dispar [ 18 ] and the malaria mosquito Anopheles stephensi [ 19 ] in response to viral, bacterial and fungal challenged, respectively. In contrast, gut bacteria in the honey bee Apis mellifera [ 20 ] and cockroach Blattella germanica [ 21 ] could protect their hosts against invading pathogens by up-regulated the host immune response or by producing antimicrobial compounds.…”

“…The insect gut is a complex ecosystem consisting of diverse communities of microbes that play important roles in host physiology including nutrition metabolism, immunity modulation and pathogen defense [ 15 ]. Recent studies have shown that insect gut microbiota could affect to the pathogenic process and the pesticidal efficiency of insect pathogens [ 16 , 17 , 18 , 19 , 20 , 21 ]. For example, gut microbiota of the beet armyworm Spodoptera exigua could enhance baculovirus virulence by modulating gut immunity [ 16 ].…”

Role of Insect Gut Microbiota in Pesticide Degradation: A Review

“…Firmicutes are found in the digestive tracts of many lepidopteran larvae, even though the digestive tracts of larvae are suggested to be not very suitable for bacteria to live. This includes Spodoptera litura Fabricius ( Thakur et al, 2016 ), Manduca sexta Linnaeus ( Holt, 2013 ), Helicoverpa armigera Hubner ( Yuan et al, 2021 ), and many other lepidopteran species ( Mereghetti et al, 2017 ; Gomes et al, 2020 ). Bacteria belonging to the genus Enterococcus are known to create a variety of bacteriocins, which are potent antibacterial chemicals that can influence the composition of the gut microbial communities ( Van Arnam et al, 2018 ).…”

Similar Bacterial Communities among Different Populations of a Newly Emerging Invasive Species, Tuta absoluta (Meyrick)

“…Lepidopteran insect guts generally contain abundant microorganisms [ 14 , 15 ]. Several studies have investigated the intestinal bacterial communities of lepidopterans, such as Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) [ 16 , 17 , 18 ], Spodoptera littoralis (Boisd.) (Lep.…”

“…: Saturniidae) [ 29 ]. Meanwhile, gut microbiota of these insects are significantly affected by developmental stage [ 19 , 21 ], food/host plant type [ 26 , 27 , 28 , 30 , 31 , 32 ], geographical location [ 23 , 29 ], environment [ 12 , 33 ], and pathogen invasion [ 18 ]. Even though the microbiota of several distinct feeding guilds, including foliage feeder and fruit borer, have been explored, little is known about that of lepidopteran leaf miners.…”