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      Enzyme Activities at Different Stages of Plant Biomass Decomposition in Three Species of Fungus-Growing Termites

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          ABSTRACT

          Fungus-growing termites rely on mutualistic fungi of the genus Termitomyces and gut microbes for plant biomass degradation. Due to a certain degree of symbiont complementarity, this tripartite symbiosis has evolved as a complex bioreactor, enabling decomposition of nearly any plant polymer, likely contributing to the success of the termites as one of the main plant decomposers in the Old World. In this study, we evaluated which plant polymers are decomposed and which enzymes are active during the decomposition process in two major genera of fungus-growing termites. We found a diversity of active enzymes at different stages of decomposition and a consistent decrease in plant components during the decomposition process. Furthermore, our findings are consistent with the hypothesis that termites transport enzymes from the older mature parts of the fungus comb through young worker guts to freshly inoculated plant substrate. However, preliminary fungal RNA sequencing (RNA-seq) analyses suggest that this likely transport is supplemented with enzymes produced in situ. Our findings support that the maintenance of an external fungus comb, inoculated with an optimal mixture of plant material, fungal spores, and enzymes, is likely the key to the extraordinarily efficient plant decomposition in fungus-growing termites.

          IMPORTANCE Fungus-growing termites have a substantial ecological footprint in the Old World (sub)tropics due to their ability to decompose dead plant material. Through the establishment of an elaborate plant biomass inoculation strategy and through fungal and bacterial enzyme contributions, this farming symbiosis has become an efficient and versatile aerobic bioreactor for plant substrate conversion. Since little is known about what enzymes are expressed and where they are active at different stages of the decomposition process, we used enzyme assays, transcriptomics, and plant content measurements to shed light on how this decomposition of plant substrate is so effectively accomplished.

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          Most cited references 59

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          Symbiotic digestion of lignocellulose in termite guts.

           Andreas Brune (2014)
          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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            Cell-wall carbohydrates and their modification as a resource for biofuels.

            Plant cell walls represent the most abundant renewable resource on this planet. Despite their great abundance, only 2% of this resource is currently used by humans. Hence, research into the feasibility of using plant cell walls in the production of cost-effective biofuels is desirable. The main bottleneck for using wall materials is the recalcitrance of walls to efficient degradation into fermentable sugars. Manipulation of the wall polysaccharide biosynthetic machinery or addition of wall structure-altering agents should make it possible to tailor wall composition and architecture to enhance sugar yields upon wall digestion for biofuel fermentation. Study of the biosynthetic machinery and its regulation is still in its infancy and represents a major scientific and technical research challenge. Of course, any change in wall structure to accommodate cost-efficient biofuel production may have detrimental effects on plant growth and development due to the diverse roles of walls in the life of a plant. However, the diversity and abundance of wall structures present in the plant kingdom gives hope that this challenge can be met.
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              Aspergillus Enzymes Involved in Degradation of Plant Cell Wall Polysaccharides

              Degradation of plant cell wall polysaccharides is of major importance in the food and feed, beverage, textile, and paper and pulp industries, as well as in several other industrial production processes. Enzymatic degradation of these polymers has received attention for many years and is becoming a more and more attractive alternative to chemical and mechanical processes. Over the past 15 years, much progress has been made in elucidating the structural characteristics of these polysaccharides and in characterizing the enzymes involved in their degradation and the genes of biotechnologically relevant microorganisms encoding these enzymes. The members of the fungal genus Aspergillus are commonly used for the production of polysaccharide-degrading enzymes. This genus produces a wide spectrum of cell wall-degrading enzymes, allowing not only complete degradation of the polysaccharides but also tailored modifications by using specific enzymes purified from these fungi. This review summarizes our current knowledge of the cell wall polysaccharide-degrading enzymes from aspergilli and the genes by which they are encoded.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Appl Environ Microbiol
                Appl. Environ. Microbiol
                aem
                aem
                AEM
                Applied and Environmental Microbiology
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                0099-2240
                1098-5336
                21 December 2017
                14 February 2018
                1 March 2018
                14 February 2018
                : 84
                : 5
                Affiliations
                [a ]Centre for Social Evolution, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark
                [b ]Department of Chemical and Biochemical Engineering, Technical University of Denmark, Kongens Lyngby, Denmark
                [c ]Laboratory of Genetics, Wageningen University, Wageningen, The Netherlands
                [d ]Department of Plant and Environmental Sciences, Section for Plant Glycobiology, University of Copenhagen, Frederiksberg, Denmark
                [e ]Carlsberg Research Laboratory, Copenhagen, Denmark
                University of Georgia
                Author notes
                Address correspondence to Rafael R. da Costa, Rafael.dacosta@ 123456bio.ku.dk .

                Citation da Costa RR, Hu H, Pilgaard B, Vreeburg SME, Schückel J, Pedersen KSK, Kračun SK, Busk PK, Harholt J, Sapountzis P, Lange L, Aanen DK, Poulsen M. 2018. Enzyme activities at different stages of plant biomass decomposition in three species of fungus-growing termites. Appl Environ Microbiol 84:e01815-17. https://doi.org/10.1128/AEM.01815-17.

                Article
                01815-17
                10.1128/AEM.01815-17
                5812949
                29269491
                Copyright © 2018 da Costa et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Page count
                supplementary-material: 1, Figures: 3, Tables: 4, Equations: 0, References: 68, Pages: 16, Words: 10357
                Product
                Funding
                Funded by: Villum Fonden (Villum Foundation), https://doi.org/10.13039/100008398;
                Award ID: 10101
                Award Recipient :
                Funded by: Carlsbergfondet (Carlsberg Foundation), https://doi.org/10.13039/501100002808;
                Award Recipient :
                Funded by: Governo Brasil (Brazilian Government), https://doi.org/10.13039/501100002425;
                Award ID: 13240/13-7
                Award Recipient :
                Categories
                Microbial Ecology
                Custom metadata
                March 2018

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