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      Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites

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          Abstract

          Background

          Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. They mainly feed on wood and other plant material at different stages of humification. Lignocellulose is often a principal component of such plant diet, and termites largely rely on their symbiotic microbiota and associated enzymes to decompose their food efficiently. While lower termites and their gut flagellates were given larger scientific attention in the past, the gut lignocellulolytic bacteria of higher termites remain less explored. Therefore, in this study, we investigated the structure and function of gut prokaryotic microbiomes from 11 higher termite genera representative of Syntermitinae, Apicotermitinae, Termitidae and Nasutitermitinae subfamilies, broadly grouped into plant fibre- and soil-feeding termite categories.

          Results

          Despite the different compositional structures of the studied termite gut microbiomes, reflecting well the diet and host lineage, we observed a surprisingly high functional congruency between gut metatranscriptomes from both feeding groups. The abundance of transcripts encoding for carbohydrate active enzymes as well as expression and diversity profiles of assigned glycoside hydrolase families were also similar between plant fibre- and soil-feeding termites. Yet, dietary imprints highlighted subtle metabolic differences specific to each feeding category. Roughly, 0.18% of de novo re-constructed gene transcripts were shared between the different termite gut microbiomes, making each termite gut a unique reservoir of genes encoding for potentially industrially applicable enzymes, e.g. relevant to biomass degradation. Taken together, we demonstrated the functional equivalence in microbial populations across different termite hosts.

          Conclusions

          Our results provide valuable insight into the bacterial component of the termite gut system and significantly expand the inventory of termite prokaryotic genes participating in the deconstruction of plant biomass.

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          Most cited references34

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          Horizontal gene transfer in prokaryotes: quantification and classification.

          Comparative analysis of bacterial, archaeal, and eukaryotic genomes indicates that a significant fraction of the genes in the prokaryotic genomes have been subject to horizontal transfer. In some cases, the amount and source of horizontal gene transfer can be linked to an organism's lifestyle. For example, bacterial hyperthermophiles seem to have exchanged genes with archaea to a greater extent than other bacteria, whereas transfer of certain classes of eukaryotic genes is most common in parasitic and symbiotic bacteria. Horizontal transfer events can be classified into distinct categories of acquisition of new genes, acquisition of paralogs of existing genes, and xenologous gene displacement whereby a gene is displaced by a horizontally transferred ortholog from another lineage (xenolog). Each of these types of horizontal gene transfer is common among prokaryotes, but their relative contributions differ in different lineages. The fixation and long-term persistence of horizontally transferred genes suggests that they confer a selective advantage on the recipient organism. In most cases, the nature of this advantage remains unclear, but detailed examination of several cases of acquisition of eukaryotic genes by bacteria seems to reveal the evolutionary forces involved. Examples include isoleucyl-tRNA synthetases whose acquisition from eukaryotes by several bacteria is linked to antibiotic resistance, ATP/ADP translocases acquired by intracellular parasitic bacteria, Chlamydia and Rickettsia, apparently from plants, and proteases that may be implicated in chlamydial pathogenesis.
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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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              Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes.

              Ten years ago, the discovery of Mimivirus, a virus infecting Acanthamoeba, initiated a reappraisal of the upper limits of the viral world, both in terms of particle size (>0.7 micrometers) and genome complexity (>1000 genes), dimensions typical of parasitic bacteria. The diversity of these giant viruses (the Megaviridae) was assessed by sampling a variety of aquatic environments and their associated sediments worldwide. We report the isolation of two giant viruses, one off the coast of central Chile, the other from a freshwater pond near Melbourne (Australia), without morphological or genomic resemblance to any previously defined virus families. Their micrometer-sized ovoid particles contain DNA genomes of at least 2.5 and 1.9 megabases, respectively. These viruses are the first members of the proposed "Pandoravirus" genus, a term reflecting their lack of similarity with previously described microorganisms and the surprises expected from their future study.
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                Author and article information

                Contributors
                magdalena.calusinska@list.lu
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                23 June 2020
                23 June 2020
                2020
                : 8
                : 96
                Affiliations
                [1 ]GRID grid.423669.c, Luxembourg Institute of Science and Technology, ; 41 rue du Brill, L-4422 Belvaux, Luxembourg
                [2 ]GRID grid.11318.3a, ISNI 0000000121496883, Université Paris 13–Sorbonne Paris Cité, ; LEEC, EA 4443 Villetaneuse, France
                [3 ]GRID grid.462844.8, ISNI 0000 0001 2308 1657, iEES-Paris, Institute of Research for Development, , Sorbonne Universités, ; U 242 Bondy, France
                [4 ]GRID grid.16008.3f, ISNI 0000 0001 2295 9843, Luxembourg Centre for Systems Biomedicine, , University of Luxembourg, ; 7 avenue des Hauts-Fourneaux, L-4362 Esch-sur-Alzette, Luxembourg
                [5 ]GRID grid.4989.c, ISNI 0000 0001 2348 0746, Université Libre de Bruxelles, ; 50 avenue F.D. Roosevelt, B-1050 Brussels, Belgium
                [6 ]GRID grid.16008.3f, ISNI 0000 0001 2295 9843, University of Luxembourg, ; 2 avenue de l’Université, L-4365 Esch-sur-Alzette, Luxembourg
                Author information
                http://orcid.org/0000-0003-2270-2217
                Article
                872
                10.1186/s40168-020-00872-3
                7313118
                32576253
                59768462-b572-4e11-8d5d-1963b2da50a1
                © The Author(s) 2020

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 21 February 2020
                : 20 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001866, Fonds National de la Recherche Luxembourg;
                Award ID: C14/SR/8286517
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002661, Fonds De La Recherche Scientifique - FNRS;
                Award ID: PDR T.0065.15
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                termite gut microbiome,metatranscriptomics,16s rrna gene sequencing,isoptera,cazymes,lignocellulose decomposition

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