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      Lower Termite Associations with Microbes: Synergy, Protection, and Interplay

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          Abstract

          Lower-termites are one of the best studied symbiotic systems in insects. Their ability to feed on a nitrogen-poor, wood-based diet with help from symbiotic microbes has been under investigation for almost a century. A unique microbial consortium living in the guts of lower termites is essential for wood-feeding. Host and symbiont cellulolytic enzymes synergize each other in the termite gut to increase digestive efficiency. Because of their critical role in digestion, gut microbiota are driving forces in all aspects of termite biology. Social living also comes with risks for termites. The combination of group living and a microbe-rich habitat makes termites potentially vulnerable to pathogenic infections. However, the use of entomopathogens for termite control has been largely unsuccessful. One mechanism for this failure may be symbiotic collaboration; i.e., one of the very reasons termites have thrived in the first place. Symbiont contributions are thought to neutralize fungal spores as they pass through the termite gut. Also, when the symbiont community is disrupted pathogen susceptibility increases. These recent discoveries have shed light on novel interactions for symbiotic microbes both within the termite host and with pathogenic invaders. Lower termite biology is therefore tightly linked to symbiotic associations and their resulting physiological collaborations.

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          Most cited references77

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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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            The Gut Microbiota of Termites: Digesting the Diversity in the Light of Ecology and Evolution.

            Termite guts harbor a dense and diverse microbiota that is essential for symbiotic digestion. The major players in lower termites are unique lineages of cellulolytic flagellates, whereas higher termites harbor only bacteria and archaea. The functions of the mostly uncultivated lineages and their distribution in different diet groups are slowly emerging. Patterns in community structure match changes in the biology of different host groups and reflect the availability of microbial habitats provided by flagellates, wood fibers, and the increasing differentiation of the intestinal tract, which also creates new niches for microbial symbionts. Whereas the intestinal communities in the closely related cockroaches seem to be shaped primarily by the selective forces of microhabitat and functional niche, the social behavior of termites reduces the stochastic element of community assembly, which facilitates coevolution and may ultimately result in cospeciation.
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              Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut.

              Termites harbor diverse symbiotic gut microorganisms, the majority of which are as yet uncultivable and their interrelationships unclear. Here, we present the complete genome sequence of the uncultured Bacteroidales endosymbiont of the cellulolytic protist Pseudotrichonympha grassii, which accounts for 70% of the bacterial cells in the gut of the termite Coptotermes formosanus. Functional annotation of the chromosome (1,114,206 base pairs) unveiled its ability to fix dinitrogen and recycle putative host nitrogen wastes for biosynthesis of diverse amino acids and cofactors, and import glucose and xylose as energy and carbon sources. Thus, nitrogen fixation and cellulolysis are coupled within the protist's cells. This highly evolved symbiotic system probably underlies the ability of the worldwide pest termites Coptotermes to use wood as their sole food.
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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
                08 April 2016
                2016
                : 7
                : 422
                Affiliations
                [1]Department of Entomology, Purdue University, West Lafayette IN, USA
                Author notes

                Edited by: Christine Moissl-Eichinger, Medical University Graz, Austria

                Reviewed by: Saria Otani, Copenhagen University, Denmark; Rebeca B. Rosengaus, Northeastern University, USA

                *Correspondence: Brittany F. Peterson, bfpeterson@ 123456email.arizona.edu

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

                Article
                10.3389/fmicb.2016.00422
                4824777
                27092110
                787ec081-0cae-469c-b533-486746064fae
                Copyright © 2016 Peterson and Scharf.

                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
                : 08 January 2016
                : 16 March 2016
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 86, Pages: 7, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: 1233484CBET
                Funded by: Indiana Academy of Sciences 10.13039/100006974
                Award ID: 2014-13
                Categories
                Microbiology
                Mini Review

                Microbiology & Virology
                termite,digestion,immunity,insect–microbe interactions,social insect,symbiosis

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