Abstract

Evolutionary and ecological forces are important factors that shape gut microbial profiles in hosts, which can help insects adapt to different environments through modulating their metabolites. However, little is known about how gut microbes and metabolites are altered when lepidopteran pest species switch hosts. In the present study, using 16S-rDNA sequencing and mass spectrometry-based metabolomics, we analyzed the gut microbiota and metabolites of three populations of Plutella xylostella: one feeding on radish (PxR) and two feeding on peas (PxP; with PxP-1 and PxP-17 being the first and 17th generations after host shift from radish to peas, respectively). We found that the diversity of gut microbes in PxP-17 was significantly lower than those in PxR and PxP-1, which indicates a distinct change in gut microbiota after host shift. Kyoto Encyclopedia of Genes and Genomes analysis revealed that the functions of energy metabolism, signal transduction, and xenobiotics biodegradation and metabolism were increased in PxP-17, suggesting their potential roles in host adaptation. Metabolic profiling showed a significant difference in the abundance of gut metabolites between PxR and PxP-17, and significant correlations of gut bacteria with gut metabolites. These findings shed light on the interaction among plants, herbivores, and symbionts, and advance our understanding of host adaptation associated with gut bacteria and metabolic activities in P. xylostella.

Highlights

  • Bacterial symbionts are considered as “hidden players” in insect–plant interactions [1]

  • The length of the sequence reads was of 200–540 bp, with 99.92% of them being of 400–440 bp. These sequence reads were clustered into 432 bacterial operational taxonomic units (OTUs)

  • PxP-17 (17th generation of P. xylostella feeding on peas after host shift from radish) had a higher abundance of dominant bacteria but at a lower diversity compared to Plutella xylostella: one feeding on radish (PxR) (P. xylostella feeding on radish) and PxP-1 (1st generation of P. xylostella feeding on peas after host shift from radish) (Figure 1b and Figure S1b)

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Summary

Introduction

Bacterial symbionts are considered as “hidden players” in insect–plant interactions [1]. Understanding the dynamic relationships between the structure of gut microbial communities and metabolites in insects during plant host shifts can contribute to a better understanding of herbivore ecology and improve the biocontrol of insect pests. P. xylostella can rapidly adapt to peas, with larval survival rate increasing from 2.4% (first generation) to 49.7% (fourth generation). This adaptation to feeding on pea plants was identified as resulting from an autosomal oligogenic inheritance with “maternal effects” [23]. We described the gut microbial taxonomic composition in P. xylostella feeding on different host plants and predict each taxon’s metabolic function

Results
Discussion
Metabolite Extraction and Profiling
Data Analyses
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