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      Bacterial Symbionts in Lepidoptera: Their Diversity, Transmission, and Impact on the Host

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          Abstract

          The insect’s microbiota is well acknowledged as a “hidden” player influencing essential insect traits. The gut microbiome of butterflies and moths (Lepidoptera) has been shown to be highly variable between and within species, resulting in a controversy on the functional relevance of gut microbes in this insect order. Here, we aim to (i) review current knowledge on the composition of gut microbial communities across Lepidoptera and (ii) elucidate the drivers of the variability in the lepidopteran gut microbiome and provide an overview on (iii) routes of transfer and (iv) the putative functions of microbes in Lepidoptera. To find out whether Lepidopterans possess a core gut microbiome, we compared studies of the microbiome from 30 lepidopteran species. Gut bacteria of the Enterobacteriaceae, Bacillaceae, and Pseudomonadaceae families were the most widespread across species, with Pseudomonas, Bacillus, Staphylococcus, Enterobacter, and Enterococcus being the most common genera. Several studies indicate that habitat, food plant, and age of the host insect can greatly impact the gut microbiome, which contributes to digestion, detoxification, or defense against natural enemies. We mainly focus on the gut microbiome, but we also include some examples of intracellular endosymbionts. These symbionts are present across a broad range of insect taxa and are known to exert different effects on their host, mostly including nutrition and reproductive manipulation. Only two intracellular bacteria genera ( Wolbachia and Spiroplasma) have been reported to colonize reproductive tissues of Lepidoptera, affecting their host’s reproduction. We explore routes of transmission of both gut microbiota and intracellular symbionts and have found that these microbes may be horizontally transmitted through the host plant, but also vertically via the egg stage. More detailed knowledge about the functions and plasticity of the microbiome in Lepidoptera may provide novel leads for the control of lepidopteran pest species.

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          The gut bacteria of insects: nonpathogenic interactions.

          The diversity of the Insecta is reflected in the large and varied microbial communities inhabiting the gut. Studies, particularly with termites and cockroaches, have focused on the nutritional contributions of gut bacteria in insects living on suboptimal diets. The indigenous gut bacteria, however, also play a role in withstanding the colonization of the gut by non-indigenous species including pathogens. Gut bacterial consortia adapt by the transfer of plasmids and transconjugation between bacterial strains, and some insect species provide ideal conditions for bacterial conjugation, which suggests that the gut is a "hot spot" for gene transfer. Genomic analysis provides new avenues for the study of the gut microbial community and will reveal the molecular foundations of the relationships between the insect and its microbiome. In this review the intestinal bacteria is discussed in the context of developing our understanding of symbiotic relationships, of multitrophic interactions between insects and plant or animal host, and in developing new strategies for controlling insect pests.
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            Multiorganismal insects: diversity and function of resident microorganisms.

            All insects are colonized by microorganisms on the insect exoskeleton, in the gut and hemocoel, and within insect cells. The insect microbiota is generally different from microorganisms in the external environment, including ingested food. Specifically, certain microbial taxa are favored by the conditions and resources in the insect habitat, by their tolerance of insect immunity, and by specific mechanisms for their transmission. The resident microorganisms can promote insect fitness by contributing to nutrition, especially by providing essential amino acids, B vitamins, and, for fungal partners, sterols. Some microorganisms protect their insect hosts against pathogens, parasitoids, and other parasites by synthesizing specific toxins or modifying the insect immune system. Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communication; and the potential value of manipulation of the microbiota to control insect pests.
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              Plant defense against herbivores: chemical aspects.

              Plants have evolved a plethora of different chemical defenses covering nearly all classes of (secondary) metabolites that represent a major barrier to herbivory: Some are constitutive; others are induced after attack. Many compounds act directly on the herbivore, whereas others act indirectly via the attraction of organisms from other trophic levels that, in turn, protect the plant. An enormous diversity of plant (bio)chemicals are toxic, repellent, or antinutritive for herbivores of all types. Examples include cyanogenic glycosides, glucosinolates, alkaloids, and terpenoids; others are macromolecules and comprise latex or proteinase inhibitors. Their modes of action include membrane disruption, inhibition of nutrient and ion transport, inhibition of signal transduction processes, inhibition of metabolism, or disruption of the hormonal control of physiological processes. Recognizing the herbivore challenge and precise timing of plant activities as well as the adaptive modulation of the plants' metabolism is important so that metabolites and energy may be efficiently allocated to defensive activities.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                27 March 2018
                2018
                : 9
                : 556
                Affiliations
                [1] 1Institute of Biology, Freie Universität Berlin , Berlin, Germany
                [2] 2Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche Peuplements Végétaux et Bioagresseurs en Milieu Tropical , Saint-Pierre, La Réunion
                [3] 3Department for Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz , Mainz, Germany
                [4] 4Biosystematics Group, Wageningen University and Research , Wageningen, Netherlands
                Author notes

                Edited by: Sébastien Duperron, National Museum of Natural History, France

                Reviewed by: Amparo Latorre, Universitat de València, Spain; Irene Lucile Garcia Newton, Indiana University Bloomington, United States

                *Correspondence: Nina E. Fatouros, nina.fatouros@ 123456wur.nl

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2018.00556
                5881003
                29636736
                caa0b6f7-8b11-49c3-a36f-37d5b513f4fc
                Copyright © 2018 Paniagua Voirol, Frago, Kaltenpoth, Hilker and Fatouros.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 22 December 2017
                : 12 March 2018
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 147, Pages: 14, Words: 0
                Categories
                Microbiology
                Review

                Microbiology & Virology
                gut bacteria,endosymbionts,moth,butterfly,symbiosis,horizontal transfer,maternal transfer

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