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      Symbiont-derived β-1,3-glucanases in a social insect: mutualism beyond nutrition

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          Abstract

          Termites have had a long co-evolutionary history with prokaryotic and eukaryotic gut microbes. Historically, the role of these anaerobic obligate symbionts has been attributed to the nutritional welfare of the host. We provide evidence that protozoa (and/or their associated bacteria) colonizing the hindgut of the dampwood termite Zootermopsis angusticollis, synthesize multiple functional β-1,3-glucanases, enzymes known for breaking down β-1,3-glucans, the main component of fungal cell walls. These enzymes, we propose, may help in both digestion of ingested fungal hyphae and protection against invasion by fungal pathogens. This research points to an additional novel role for the mutualistic hindgut microbial consortia of termites, an association that may extend beyond lignocellulolytic activity and nitrogen fixation to include a reduction in the risks of mycosis at both the individual- and colony-levels while nesting in and feeding on microbial-rich decayed wood.

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          Most cited references51

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          Social immunity.

          Social insect colonies have evolved collective immune defences against parasites. These 'social immune systems' result from the cooperation of the individual group members to combat the increased risk of disease transmission that arises from sociality and group living. In this review we illustrate the pathways that parasites can take to infect a social insect colony and use these pathways as a framework to predict colony defence mechanisms and present the existing evidence. We find that the collective defences can be both prophylactic and activated on demand and consist of behavioural, physiological and organisational adaptations of the colony that prevent parasite entrance, establishment and spread. We discuss the regulation of collective immunity, which requires complex integration of information about both the parasites and the internal status of the insect colony. Our review concludes with an examination of the evolution of social immunity, which is based on the consequences of selection at both the individual and the colony level.
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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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              Gut microbiome-host interactions in health and disease

              The gut microbiome is the term given to describe the vast collection of symbiotic microorganisms in the human gastrointestinal system and their collective interacting genomes. Recent studies have suggested that the gut microbiome performs numerous important biochemical functions for the host, and disorders of the microbiome are associated with many and diverse human disease processes. Systems biology approaches based on next generation 'omics' technologies are now able to describe the gut microbiome at a detailed genetic and functional (transcriptomic, proteomic and metabolic) level, providing new insights into the importance of the gut microbiome in human health, and they are able to map microbiome variability between species, individuals and populations. This has established the importance of the gut microbiome in the disease pathogenesis for numerous systemic disease states, such as obesity and cardiovascular disease, and in intestinal conditions, such as inflammatory bowel disease. Thus, understanding microbiome activity is essential to the development of future personalized strategies of healthcare, as well as potentially providing new targets for drug development. Here, we review recent metagenomic and metabonomic approaches that have enabled advances in understanding gut microbiome activity in relation to human health, and gut microbial modulation for the treatment of disease. We also describe possible avenues of research in this rapidly growing field with respect to future personalized healthcare strategies.
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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
                21 November 2014
                2014
                : 5
                : 607
                Affiliations
                [1] 1Department of Marine and Environmental Sciences, Northeastern University Boston, MA, USA
                [2] 2Department of Biological Sciences, Towson University Towson, MD, USA
                [3] 3Department of Biology, Northeastern University Boston, MA, USA
                Author notes

                Edited by: Spencer V. Nyholm, University of Connecticut, USA

                Reviewed by: Robert W. Thacker, University of Alabama at Birmingham, USA; Kenneth Noll, University of Connecticut, USA

                *Correspondence: Rebeca B. Rosengaus, Department of Marine and Environmental Sciences, Northeastern University, 134 Mugar Life Sciences Building, 360 Huntington Avenue, Boston, MA 02115-5000, USA e-mail: r.rosengaus@ 123456neu.edu

                Present address: Ryan W. Benson, Forsyth Institute, Cambridge, MA, USA

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

                Article
                10.3389/fmicb.2014.00607
                4240165
                25484878
                fd1cfb8b-4df0-4747-82d3-06595736d0d5
                Copyright © 2014 Rosengaus, Schultheis, Yalonetskaya, Bulmer, DuComb, Benson, Thottam and Godoy-Carter.

                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
                : 01 September 2014
                : 24 October 2014
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 59, Pages: 11, Words: 0
                Categories
                Microbiology
                Original Research Article

                Microbiology & Virology
                gut protozoa,disease resistance,β-1,3-glucanases,termites,social immunity,mycosis
                Microbiology & Virology
                gut protozoa, disease resistance, β-1, 3-glucanases, termites, social immunity, mycosis

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