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

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.

The Tripartite Interaction of Host Immunity–Bacillus thuringiensis Infection–Gut Microbiota

“…It suggests that different microbial species may have a different regulatory function in the host. Similar to the above results, the gut commensal microbiota of Red palm weevil (RPW), Rhynchophorus ferrugineus Olivier can help to protect against pathogenic infection by priming the immune system [ 44 ], and the colonization of gut commensal microbiota could enhance the immunocompetence of the host. Futo et al (2016) reported that Tribolium castaneum larvae with less microbiota load showed a decrease in survival rate upon immune challenge by Bt [ 45 ], which indicates that gut microbiota is essential for immune priming.…”

Transcriptome and gene expression analysis ofRhynchophorus ferrugineus(Coleoptera: Curculionidae) during developmental stages

“…Although multiple researches have been done to find new ways to control R. ferrugineus , including chemical agents ( Pugliese et al, 2017 ; Wakil et al, 2018 ), biological agents ( Zulkifli, Zakeri & Azmi, 2018 ), and intestinal microbes ( Habineza et al., 2019 ; Muhammad et al, 2019 ), the results are not effective. There are few studies on the molecular characteristics of R. ferrugineus , including transcriptome, genome structure and proteome ( Muhammad et al, 2019 ). Transcriptomics provides complementary data and gene expression data for available genomes for organisms at specific conditions or at different stages of development.…”

“…This feeding behavior renders detection of the pest difficult until it is already too late, and most traditional methods of pest control, including chemical pesticides, ineffective ( Ferry & Gomez, 2002 ; Faleiro, 2006 ; Faleiro et al, 2012 ). Recent studies showed that gut microbiota influenced the development of red palm weevil by regulating nutrient metabolism ( Habineza et al., 2019 ), and understanding the immune stimulating effect of intestinal commensal bacteria on larvae will be beneficial to the formulation of its control strategy ( Muhammad et al, 2019 ). The use of biological control methods to prevent the R. ferrugineus (mainly microbes) has achieved certain success, but the application still needs a long time ( Mazza et al, 2014 ).…”

Gut Bacteria in the Holometabola: A Review of Obligate and Facultative Symbionts

“…The very development of the immune system is enhanced by gut bacteria ( Tables 1–4 ). Facultative bacteria aid in immune system homeostasis in fruit flies and honeybees ( Ryu et al 2008 , Kwong et al 2017 ), and in immune system priming in the red palm weevil ( Muhammad et al 2019 ). Infestations by parasitic eukaryotes are reduced by symbiont-mediated immune priming: trypanosomatids are combated in bumblebees ( Bombus ) (Latreille, Hymenoptera: Apidae) harboring core facultative symbionts ( Koch and Schmid-Hempel 2011 ), and in mosquitoes, the infection rate of the malaria parasite Plasmodium (Marchiafava and Celli, Haemospororida: Plasmodiidae) is lessened by the presence of a facultative bacterial microbiome ( Dong et al 2009 ).…”