Toward an Integrated Understanding of the Lepidoptera Microbiome

Shao, Yongqi; Mason, Charles J.; Felton, Gary W.

doi:10.1146/annurev-ento-020723-102548

Cited by 18 publications

(6 citation statements)

References 131 publications

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“…Our results are supportive of elucidating the co-evolution of gut bacteria and insect hosts. The review focused on the Lepidoptera microbiome also summarizes many examples of gut microbiota mediating host insect detoxification of plant toxins and xenobiotics ( 65 ), which is a strong support for our conclusion. Second, since the degradation of kaempferol might not be specific to EbPXG5, we did not exclude other bacteria that may degrade kaempferol in this study.…”

Section: Discussionsupporting

confidence: 65%

Gut bacteria mediated adaptation of diamondback moth, Plutella xylostella, to secondary metabolites of host plants

Xia,

Wang,

Gurr

et al. 2023

mSystems

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The diamondback moth (DBM), Plutella xylostella, has successfully adapted to the potent chemical defenses of Brassicaceae plants that deter most other herbivores. Gut bacteria are increasingly recognized as key to the biology of many species but their role in DBM adaptation to plant defense compounds is not well known. In this study, the secondary metabolites of radish seedlings, rich in flavonoids, were identified by liquid chromatography-mass spectrometry. These secondary metabolites reduced the larval growth of DBM lacking gut bacteria. The effect was rapidly eclipsed by the re-introduction of gut microbiota, which was dominated by Enterobacter (Proteobacteria). Similarly, while treatment with the flavonoid kaempferol adversely affected growth and extended the development time, these were alleviated by the re-introduction of Enterobacter sp. EbPXG5 (EbPXG5) to the DBM gut. EbPXG5 not only degrades kaempferol both in vitro and DBM gut, but is also shown to colonize the gut epithelium, forming a protective biofilm. Genomic sequencing of EbPXG5 showed that metabolic genes were the most abundant, especially those involved in xenobiotic degradation, and the metabolism of terpenoids and polyketides, which could participate in the degradation of plant secondary metabolites such as kaempferol. Overall, our results showed that EbPXG5 is a bacterium common in the gut of DBM larvae and has the in vitro and in vivo capacity to detoxify a major secondary metabolite that is produced in brassica plants as a defense against herbivores. This insect-bacterial association may be an important contributor to the status of DBM as a major pest of brassica crops worldwide. IMPORTANCE In this study, we identify an important role of gut bacteria in mediating the adaptation of diamondback moth (DBM) to plant secondary metabolites. We demonstrate that kaempferol’s presence in radish seedlings greatly reduces the fitness of DBM with depleted gut biota. Reinstatement of gut biota, particularly Enterobacter sp. EbPXG5, improved insect performance by degrading kaempferol. This bacterium was common in the larval gut of DBM, lining the epithelium as a protective film. Our work highlights the role of symbiotic bacteria in insect herbivore adaptation to plant defenses and provides a practical and mechanistic framework for developing a more comprehensive understanding of insect-gut microbe-host plant co-evolution.

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Section: Discussionsupporting

confidence: 65%

Gut bacteria mediated adaptation of diamondback moth, Plutella xylostella, to secondary metabolites of host plants

Xia,

Wang,

Gurr

et al. 2023

mSystems

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“…Research on the growth dynamics and gut symbionts of lepidopterans is of special relevance given their status as economically important pests and the uncertainty surrounding the functions of their microbiomes ( Voirol et al 2018 , Shao et al 2023 ) In this study, we compared the growth and development of S. exigua larvae reared on alfalfa and wheat germ diets in the presence and absence of streptomycin antibiotic. Using a metabarcoding approach our study allowed the identification of the metabolically active bacteria from the pool of total gut bacteria present, and how they vary with diet and antibiotics.…”

Section: Discussionmentioning

confidence: 99%

The effect of diet composition on the diversity of active gut bacteria and on the growth of Spodoptera exigua (Lepidoptera: Noctuidae)

Mugo-Kamiri,

Querejeta,

Raymond

et al. 2024

Journal of Insect Science

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Gut microbiota plays a functional role in nutrition among several insects. However, the situation is unclear in Lepidoptera. Field studies suggest the microbiome may not be stable and is determined by diet, while in the laboratory, Lepidoptera are routinely reared on diet containing antibiotics with unknown effects on microbial communities. Furthermore, molecular approaches for the characterization of lepidopteran microbiomes rarely describe the metabolically active gut bacteria. The aim of this study was to evaluate how diet and antibiotics affect Spodoptera exigua (Hübner) growth and the diversity and activity of the gut bacteria community. We assessed how alfalfa and wheat germ-based diets affected larval growth, in the presence and absence of streptomycin. Alfalfa diet improved larval growth, pupal mass, and survival, but antibiotic was only beneficial in the wheat germ diet. We observed diet-driven changes in the gut bacterial communities. In the active community, the alfalfa colony was dominated by Enterococcus and Rhodococcus whereas in the wheat germ colony, only Enterococcus was present. In contrast, spore-forming Bacilli species were very common members of the DNA community. In both cases, streptomycin had a selective effect on the relative abundance of the taxa present. Our study highlights the importance of characterizing both the diversity and activity of the gut microbiota community. DNA-derived communities may include environmental DNA, spores, or non-viable bacteria, while RNA-derived communities are more likely to give an accurate representation of the diversity of active members that are potentially directly involved in the metabolic processes of the host.

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“…Additionally, the transcriptional profiles of all cell types were substantially affected, with significant upregulation of genes involved in various metabolic processes [ 109 ]. This technology should be applied to other insect taxa to uncover the mechanisms of insect digestion and cell types involved in the process, as well as gut microbiota that can contribute significantly to the hosts’ performance, such as host nutrition, physiology, and behavior [ 119 , 120 , 121 , 122 ]. Further, it is recommended that studies should be carried out on different types of feed, uptake of pesticides, and the interaction of gut microbiota with the host or other environmental pollutants to unveil the cellular response of the insect midgut to a variety of foods and chemicals at single-cell level.…”

Section: Single-cell Transcriptomics In Insects: Applicationsmentioning

confidence: 99%

Insect Insights at the Single-Cell Level: Technologies and Applications

Sun,

Shao,

Iqbal

2023

Cells

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Single-cell techniques are a promising way to unravel the complexity and heterogeneity of transcripts at the cellular level and to reveal the composition of different cell types and functions in a tissue or organ. In recent years, advances in single-cell RNA sequencing (scRNA-seq) have further changed our view of biological systems. The application of scRNA-seq in insects enables the comprehensive characterization of both common and rare cell types and cell states, the discovery of new cell types, and revealing how cell types relate to each other. The recent application of scRNA-seq techniques to insect tissues has led to a number of exciting discoveries. Here we provide an overview of scRNA-seq and its application in insect research, focusing on biological applications, current challenges, and future opportunities to make new discoveries with scRNA-seq in insects.

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Toward an Integrated Understanding of the Lepidoptera Microbiome

Cited by 18 publications

References 131 publications

Gut bacteria mediated adaptation of diamondback moth, Plutella xylostella, to secondary metabolites of host plants

Gut bacteria mediated adaptation of diamondback moth, Plutella xylostella, to secondary metabolites of host plants

The effect of diet composition on the diversity of active gut bacteria and on the growth of Spodoptera exigua (Lepidoptera: Noctuidae)

Insect Insights at the Single-Cell Level: Technologies and Applications

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