The Promoting Effect of Gut Microbiota on Growth and Development of Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Dryophthoridae) by Modulating Its Nutritional Metabolism.

Prosper Habineza,Rong Xiao,Abrar Muhammad,Youming Hou,Xianyuan Yin,Tianliang Ji,Zhanghong Shi

doi:10.3389/fmicb.2019.01212

Prosper Habineza, Rong Xiao + Show 5 more

Open Access

https://doi.org/10.3389/fmicb.2019.01212

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Abstract

Red palm weevil (RPW), Rhynchophorus ferrugineus Olivier, is a destructive pest for palm trees worldwide. Recent studies have shown that RPW gut is colonized by microbes and alterations in gut microbiota can significantly modify its hemolymph nutrition content. However, the exact effects of gut microbiota on RPW phenotype and the underlying mechanisms remain elusive. Here germ-free (GF) RPW larvae were generated from dechorionated eggs which were reared on sterilized artificial food under axenic conditions. Compared with controls, the larval development of GF RPW individuals was markedly depressed and their body mass was reduced as well. Furthermore, the content of hemolymph protein, glucose and triglyceride were dropped significantly in GF RPW larvae. Interestingly, introducing gut microbiota into GF individuals could significantly increase the levels of the three nutrition indices. Additionally, it has also been demonstrated that RPW larvae monoassociated with Lactococcus lactis exhibited the same level of protein content with the CR (conventionally reared) insects while feeding Enterobacter cloacae to GF larvae increased their hemolymph triglyceride and glucose content markedly. Consequently, our findings suggest that gut microbiota profoundly affect the development of this pest by regulating its nutrition metabolism and different gut bacterial species show distinct impact on host physiology. Taken together, the establishment of GF and gnotobiotic RPW larvae will advance the elucidation of molecular mechanisms behind the interactions between RPW and its gut microbiota.

Highlights

It is ubiquitous that animal hosts, including insects, have established symbiotic interactions with microbes
The culture-dependent validations revealed that the greatest quantity of bacterial colonies was found in guts of conventionally reared (CR) group, followed by dechorionated eggs + food without antibiotics (DNA) and non-dechorionated eggs + food with antibiotics (NDA), while no bacterial colony was detected in GF group (Figures 1A,B)
PCR diagnosis based on bacterial 16S rRNA uncovered that the expected bands, with the size of about 1500 bp, only missed in the GF group, indicating that the guts of GF Red palm weevil (RPW) larvae was not colonized by any bacteria species (Figure 1C)

Summary

Introduction

It is ubiquitous that animal hosts, including insects, have established symbiotic interactions with microbes. Gut microbiota derived short chain fatty acids (SCFAs) have been confirmed to be crucial for host health by executing important metabolic functions (Canfora et al, 2015; Koh et al, 2016; Fellows et al, 2018). These metabolites are recognized by specific G protein-coupled receptors on enteroendocrine cells, and these cells release small enteroendocrine peptides to modulate local and systemic lipid and carbohydrate metabolism to maintain host homeostasis (Bolognini et al, 2016; Miyamoto et al, 2016). Given the pivotal effects of gut microbiota on hosts, it is of great significance to investigate the mechanisms underlying the interactions between pests and their gut microbiota which will uncover the novel potential target to boost the development of new promising management tactics on these notorious pests by disrupting these symbiotic associations

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