Transcriptomics Reveal the Survival Strategies of Enterococcus mundtii in the Gut of Spodoptera littoralis

Mazumdar, Tilottama; Teh, Beng Soon; Murali, Aishwarya; Schmidt‐Heck, Wolfgang; Schlenker, Yvonne; Vogel, Heiko; Boland, Wilhelm

doi:10.1007/s10886-021-01246-1

Cited by 20 publications

(19 citation statements)

References 85 publications

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“…The gut microbial communities of lepidopterans should be similar to the microbiota of the food ingested. But other investigations showed lepidopterans hosted a core microbial community in their guts, which was distinctive from that obtained from the food source ( Mason et al, 2020 ; Mazumdar et al, 2021 ). The importance of microorganisms in larval lepidopterans is presently debatable.…”

Section: Introductionmentioning

confidence: 78%

The Gut Microbiota Composition of Cnaphalocrocis medinalis and Their Predicted Contribution to Larval Nutrition

Li¹,

Han²,

Sun³

et al. 2022

Front. Microbiol.

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Intestinal bacterial flora plays an important role in the nutrition, physiology, and behavior of herbivorous insects. The composition of gut microbiota may also be affected by the food consumed. Cnaphalocrocis medinalis is an oligophagous pest, feeds on rice leaves almost exclusively and causes serious damage to rice in Asian countries. Using antibiotic treatment and metagenome sequencing, we investigated the influence of the food sources (rice and maize seedlings) on the structure and functions of intestinal bacteria of C. medinalis. Firstly, food utilization indices, relative growth rate (RGR), relative consumption rate (RCR), efficiency of conversion of ingested food (ECI), and efficiency of conversion of digested food (ECD), were all significantly adversely affected in the antibiotic treatment eliminating gut bacteria, showing that the microbiota loading in the gut were essential for the larva growth and development of C. medinalis. Further, metagenome sequencing revealed that different diets caused a variation in gut microbiota composition of C. medinalis, indicating that the gut microbiota were in part driven by the diet provided. However, the larvae of C. medinalis hosted a core microbial community in the gut, which was independent from the diets changing. The dominant bacteria in the two feeding groups were highly consistent in the gut of C. medinalis larvae, with the gut bacterial community dominated by Firmicutes at the phylum level, Enterococcus at the genus level, Enterococcus sp. FDAARGOS-375, E. casseliflavus, E. gallinarum, and E. sp. CR-Ec1 accounted for more than 96% of the gut microbiota. Functional prediction analysis demonstrated that gut bacteria encoded a series of metabolism-related enzymes involved in carbohydrate metabolism and amino acid synthesis. Carbohydrate metabolism was the most enriched function in both groups and was more abundant in rice feeding group than in maize feeding group. The core dominant Enterococcus species possessed complete pathways of 14 carbohydrates metabolism, 11 amino acids biosynthesis, and two vitamins synthesize, implied to contribute an essential role to the nutrition intake and development of C. medinalis. Finally, the study may provide an in-depth analysis of the symbiont-host co-adaptation and new insights into the management of C. medinalis.

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Section: Introductionmentioning

confidence: 78%

The Gut Microbiota Composition of Cnaphalocrocis medinalis and Their Predicted Contribution to Larval Nutrition

Li¹,

Han²,

Sun³

et al. 2022

Front. Microbiol.

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“…E. casseliflavus can support house fly larval development and colonize the gut of teneral adults to various degrees ( Anuradha et al., 2014 ). E. mundtii with adherence properties can form a biofilm layer on the gut wall to help insect adapt to altered environments ( Mazumdar et al., 2021b ). Probiotic characterization of E. mundtii was observed from larval gut of Plutella xylostella ( Mazumdar et al., 2021a ).…”

Section: Discussionmentioning

confidence: 99%

High nitrogen in maize enriches gut microbiota conferring insecticide tolerance in lepidopteran pest Spodoptera litura

Sun

et al. 2022

iScience

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Summary Abuse of chemical fertilizers and insecticides has created many environmental and human health hazards. We hypothesized that high nitrogen (N) in crops changes insect gut microbiota leading to enhanced insecticide tolerance. We investigated the effect of high N in maize on gut microbiota and insecticide tolerance of the polyphagous pest Spodoptera litura . Bioassays showed that high N applied in both maize plants and artificial diets significantly enhanced larval growth but reduced larval sensitivity to the insecticide methomyl. High N promoted the gut bacterial abundance in the genus Enterococcus . Inoculation with two strains ( E. mundtii and E. casseliflavus ) isolated from the larval guts increased larval tolerance to methomyl. Incorporation of antibiotics in a high-N diet increased the larval sensitivity to methomyl. These findings suggest that excessive application of N fertilizer to crops can increase insecticide tolerance of insect pests via changing gut microbiota, leading to increased use of insecticides worldwide.

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“…The other scenario that our results put forward is that specific members of Enterococcus could have an impact in reducing larval growth rate. Enterococci are lactic acid bacteria well adapted to survival in the harsh gut environment by evading host defences (Fiore et al 2019, Mazumdar et al 2021) and commonly found in Lepidoptera throughout their life cycle (Hammer et al 2014, Chen et al 2016, Teh et al 2016, González-Serrano et al 2020). The specific enterococci we detected in connection to slower growth clustered with E. casseliflavus and E. gallinarum , which can be the dominant bacteria in Lepidoptera (Martin & Mundt 1972, Tang et al 2012, Shao et al 2014, Jones et al 2019).…”

Section: Discussionmentioning

confidence: 99%

Host’s genetic background determines the outcome of reciprocal faecal transplantation on life-history traits and microbiome composition

Juottonen

Moghadam

Murphy

et al. 2022

Preprint

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Background: Microbes play a role in fundamental ecological, chemical, and physiological processes of their host. Host life-history traits from defence to growth are therefore determined not only by abiotic environment and genotype but also by microbiota composition. However, the relative importance and interactive effects of these factors may vary between organisms. Such connections remain particularly elusive in Lepidoptera, which have been argued to lack a permanent microbiome and have microbiota primarily determined by their diet and environment. We tested the microbiome specificity and its influence on life-history traits of two colour genotypes of the wood tiger moth (Arctia plantaginis) that differ in several traits, including growth. All individuals were grown in the laboratory for several generations with standardised conditions. We analysed the bacterial community of the genotypes before and after a reciprocal frass (i.e., larval faeces) transplantation and followed growth rate, pupal mass, and the production of defensive secretion. Results: After transplantation, the fast-growing genotype grew at a significantly slower rate compared to the controls, but the slow-growing genotype did not change its growth rate. The frass transplant also increased the volume of defensive secretions in the fast-growing genotype but did not affect pupal mass. Overall, the fast-growing genotype appeared more susceptible to the transplantation than the slow-growing genotype. Microbiome differences between the genotypes strongly suggest genotype-based selective filtering of bacteria from the diet and environment. A novel cluster of insect-associated Erysipelotrichaceae was exclusive to the fast-growing genotype, and specific Enterococcaceae were characteristic to the slow-growing genotype. These Enterococcaceae became more prevalent in the fast-growing genotype after the transplant, which suggests that the slower growth rate was potentially related to their presence. Conclusions: We show that some genotype-specific life-history traits in a lepidopteran host can be reversed by a reciprocal frass transplantation. The results indicate that genotype-specific selective filtering can fine-tune the bacterial community at specific life stages, particularly the larval gut, even against a background of a highly variable community with stochastic assembly. Altogether, our findings suggest that the genotype of the host can influence its susceptibility to be colonized by microbiota with impact on key life-history traits.

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Transcriptomics Reveal the Survival Strategies of Enterococcus mundtii in the Gut of Spodoptera littoralis

Cited by 20 publications

References 85 publications

The Gut Microbiota Composition of Cnaphalocrocis medinalis and Their Predicted Contribution to Larval Nutrition

The Gut Microbiota Composition of Cnaphalocrocis medinalis and Their Predicted Contribution to Larval Nutrition

High nitrogen in maize enriches gut microbiota conferring insecticide tolerance in lepidopteran pest Spodoptera litura

Host’s genetic background determines the outcome of reciprocal faecal transplantation on life-history traits and microbiome composition

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