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      Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet

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          Abstract

          Herbivores possess many counteradaptations to plant defenses, and a growing body of research describes the role of symbiotic gut bacteria in mediating herbivorous diets among insects. However, persistent bacterial symbioses have not been found in Lepidoptera, despite the fact that perhaps 99% of the species in this order are herbivorous. We surveyed bacterial communities in the guts of larvae from 31 species of lycaenid butterflies whose caterpillars had diets ranging from obligate carnivory to strict herbivory. Contrary to our expectations, we found that the bacterial communities of carnivorous and herbivorous caterpillars do not differ in richness, diversity, or composition. Many of the observed bacterial genera are commonly found in soil and plant surfaces, and we detected known homopteran endosymbionts in the guts of homopterophagous species, suggesting that larvae acquire gut bacteria from their food and environment. These results indicate that lycaenid butterflies do not rely on specific bacterial symbioses to mediate their diverse diets, and provide further evidence of taxonomically depauperate bacterial communities among Lepidoptera.

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          Most cited references57

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          Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera.

          A Douglas (1998)
          Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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            Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling.

            The symbiotic microbiota profoundly affect many aspects of host physiology; however, the molecular mechanisms underlying host-microbe cross-talk are largely unknown. Here, we show that the pyrroloquinoline quinone-dependent alcohol dehydrogenase (PQQ-ADH) activity of a commensal bacterium, Acetobacter pomorum, modulates insulin/insulin-like growth factor signaling (IIS) in Drosophila to regulate host homeostatic programs controlling developmental rate, body size, energy metabolism, and intestinal stem cell activity. Germ-free animals monoassociated with PQQ-ADH mutant bacteria displayed severe deregulation of developmental and metabolic homeostasis. Importantly, these defects were reversed by enhancing host IIS or by supplementing the diet with acetic acid, the metabolic product of PQQ-ADH.
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              Symbiotic digestion of lignocellulose in termite guts.

              Their ability to degrade lignocellulose gives termites an important place in the carbon cycle. This ability relies on their partnership with a diverse community of bacterial, archaeal and eukaryotic gut symbionts, which break down the plant fibre and ferment the products to acetate and variable amounts of methane, with hydrogen as a central intermediate. In addition, termites rely on the biosynthetic capacities of their gut microbiota as a nutritional resource. The mineralization of humus components in the guts of soil-feeding species also contributes to nitrogen cycling in tropical soils. Lastly, the high efficiency of their minute intestinal bioreactors makes termites promising models for the industrial conversion of lignocellulose into microbial products and the production of biofuels.
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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
                30 November 2016
                2016
                : 7
                : 1920
                Affiliations
                [1] 1Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge MA, USA
                [2] 2Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology Jena, Germany
                [3] 3Department of Pediatrics, University of California San Diego, La Jolla CA, USA
                [4] 4Department for Evolutionary Ecology, Johannes Gutenberg University Mainz, Germany
                Author notes

                Edited by: Thomas Carl Bosch, University of Kiel, Germany

                Reviewed by: Irene Lucile Garcia Newton, Indiana University Bloomington, USA; Nichole A. Broderick, University of Connecticut, USA

                *Correspondence: Melissa R. L. Whitaker, melliwhitaker@ 123456gmail.com Naomi E. Pierce, npierce@ 123456oeb.harvard.edu

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

                Article
                10.3389/fmicb.2016.01920
                5129467
                27965647
                7ad7cd1b-d074-45d5-a453-9edc42d49288
                Copyright © 2016 Whitaker, Salzman, Sanders, Kaltenpoth and Pierce.

                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) or licensor 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
                : 19 September 2016
                : 15 November 2016
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 105, Pages: 13, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: 1309425, DGE1144152, SES075048
                Funded by: British Ecological Society 10.13039/501100000409
                Award ID: 6007210
                Funded by: John Templeton Foundation 10.13039/100000925
                Funded by: Explorers Club 10.13039/100002861
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                lycaenidae,lepidoptera,gut microbiome,horizontal gene transfer,herbivory,aphytophagy

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