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      Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles

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          Abstract

          Symbiotic microbes can enable their host to access untapped nutritional resources but may also constrain niche space by promoting specialization. Here, we reconstruct functional changes in the evolutionary history of the symbiosis between a group of (semi-)aquatic herbivorous insects and mutualistic bacteria. Sequencing the symbiont genomes across 26 species of reed beetles (Chrysomelidae, Donaciinae) spanning four genera indicates that the genome-eroded mutualists provide life stage-specific benefits to larvae and adults, respectively. In the plant sap-feeding larvae, the symbionts are inferred to synthesize most of the essential amino acids as well as the B vitamin riboflavin. The adult reed beetles’ folivory is likely supported by symbiont-encoded pectinases that complement the host-encoded set of cellulases, as revealed by transcriptome sequencing. However, mapping the occurrence of the symbionts’ pectinase genes and the hosts’ food plant preferences onto the beetles’ phylogeny reveals multiple independent losses of pectinase genes in lineages that switched to feeding on pectin-poor plants, presumably constraining their hosts’ subsequent adaptive potential.

          Abstract

          Symbiotic microbes in insects can enable their hosts to access untapped nutritional resources. Here, the authors show that symbiotic bacteria in reed beetles can provide essential amino acids to sap-feeding larvae and help leaf-feeding adults to degrade pectin, respectively.

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          The genome of the model beetle and pest Tribolium castaneum.

          Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.
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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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              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
                mkaltenpoth@uni-mainz.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                11 June 2020
                11 June 2020
                2020
                : 11
                : 2964
                Affiliations
                [1 ]ISNI 0000 0001 1941 7111, GRID grid.5802.f, Evolutionary Ecology, Institute for Organismic and Molecular Evolution (iomE), , Johannes Gutenberg University, ; Hanns-Dieter-Hüsch-Weg 15, 55128 Mainz, Germany
                [2 ]ISNI 0000 0004 0491 7131, GRID grid.418160.a, Department of Entomology, , Max Planck Institute for Chemical Ecology, ; Hans-Knöll-Str. 8, 07745 Jena, Germany
                [3 ]ISNI 0000 0001 2230 7538, GRID grid.208504.b, Bioproduction Research Institute, , National Institute of Advanced Industrial Science and Technology, ; Tsukuba, 305-8566 Japan
                [4 ]ISNI 0000 0001 2287 2617, GRID grid.9026.d, Molekulare Evolutionsbiologie, Institut für Zoologie, , Universität Hamburg, ; Martin-Luther-King-Platz 3, 20146 Hamburg, Germany
                [5 ]ISNI 0000 0001 2190 1447, GRID grid.10392.39, Present Address: Plant Evolutionary Ecology, Institute of Evolution and Ecology, , University of Tübingen, ; Auf der Morgenstelle 5, 72076 Tübingen, Germany
                [6 ]Present Address: Maasen 6, 24107 Kiel, Germany
                Author information
                http://orcid.org/0000-0002-2918-8946
                http://orcid.org/0000-0001-5987-2602
                http://orcid.org/0000-0001-9450-0345
                Article
                16687
                10.1038/s41467-020-16687-7
                7289800
                32528063
                d968ceb6-1e3b-4dc9-9dc3-8b3dbc83e1ba
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 17 January 2020
                : 18 May 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: KI1917/1-1 and KI1917/1-2
                Award ID: KO2115/7-1 and KO2115/10-1
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100004189, Max-Planck-Gesellschaft (Max Planck Society);
                Funded by: FundRef https://doi.org/10.13039/501100000646, Japan Society for the Promotion of Science London (JSPS London);
                Award ID: Postdoctoral Fellowship for Young Scientists (JP16J40021)
                Award ID: Kakenhi grant (JP17H06388)
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100010663, EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council);
                Award ID: CoG 819585 “SYMBeetle”
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                evolutionary ecology,microbial ecology,environmental microbiology,entomology
                Uncategorized
                evolutionary ecology, microbial ecology, environmental microbiology, entomology

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