Intestinal Microbiota Confer Protection by Priming the Immune System of Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae).

Abrar Muhammad,Tianliang Ji,Prosper Habineza,Youming Hou,Zhanghong Shi

doi:10.3389/fphys.2019.01303

Abrar Muhammad, Tianliang Ji + Show 3 more

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https://doi.org/10.3389/fphys.2019.01303

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Abstract

The immune system of animals, including insects, is the vital factor to maintain the symbiotic interactions between animals and their associated microbes. However, the effects of gut microbiota on insect immunity remain mostly elusive. Red palm weevil (RPW), Rhynchophorus ferrugineus Olivier, is a destructive pest of palm trees worldwide, which has forged alliances with its gut microbiota. Here, we found that the aposymbiotic insects succumbed at a significantly faster rate than conventionally reared (CR) ones upon bacterial infection. Physiological assays confirmed that CR insects had stronger antimicrobial activity and higher phenoloxidase activity in contrast to germfree (GF) ones, indicating that the systemic immune responses of GF individuals were compromised markedly. Interestingly, under the bacterial challenge conditions, the reassociation of gut microbiota with GF insects could enhance their survival rate by rescuing their immunocompetence. Furthermore, comparative transcriptome analysis uncovered that 35 immune-related genes, including pathogen recognition receptors, effectors and immune signaling pathway, were significantly downregulated in GF insects as compared to CR ones. Collectively, our findings corrobate that intestinal commensal bacteria have profound immunostimulatory effects on RPW larvae. Therefore, knowledge on the effects of gut microbiota on RPW immune defenses may contribute to of set up efficient control strategies of this pest.

Highlights

As in vertebrates, diverse groups of microbes, being generally known as gut microbiota, colonize insect guts
Treatment cohorts of Red palm weevil (RPW) in this study were designated in four groups: (I) Conventionally reared (CR) larvae contained their inherent gut microbiota; (II) Germfree (GF) ones, being completely devoid of gut microbiota, were generated with the following steps: RPW eggs were washed in 10% sodium hypochlorite solution (NaClO) for 3–5 min, rinsed in 75% ethanol two times to remove the bacteria on the egg surface, and rinsed with sterilized distilled water two times to exclude the potential effect of sodium hypochlorite and ethanol on the following experiments
It has been previously demonstrated that RPW harbors a complex gut microbiota which is involved in the nutrition metabolism (Muhammad et al, 2017; Prosper et al, 2019)

Summary

Introduction

Diverse groups of microbes, being generally known as gut microbiota, colonize insect guts. Gut microbiota has been attested to profoundly affect host physiological traits including nutrition provision (Wong et al, 2014; Janssen and Kersten, 2015), growth and development (Blatch et al, 2010; Wong et al, 2014), mating and foraging behavior (Ami et al, 2010), and gut homeostasis (Engel and Moran, 2013; Douglas, 2015). The effects of gut microbiota on the development and proper presence of insect immunity and the mechanisms underlying gut microbiota-induced impacts on host immunity are far from being well understood, especially for the invasive insect pests

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