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      Impacts of biofilms on the conversion of cellulose

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          Abstract

          Abstract

          Lignocellulose is a widely available renewable carbon source and a promising feedstock for the production of various chemicals in biorefineries. However, its recalcitrant nature is a major hurdle that must be overcome to enable economic conversion processes. Deconstruction of lignocellulose is part of the global carbon cycle, and efficient microbial degradation systems have evolved that might serve as models to improve commercial conversion processes. Biofilms—matrix encased, spatially organized clusters of microbial cells and the predominating lifestyle in nature—have been recognized for their essential role in the degradation of cellulose in nature, e.g., in soils or in the digestive tracts of ruminant animals. Cellulolytic biofilms allow for a high concentration of enzymes at the boundary layer between the solid substrate and the liquid phase and the more complete capture of hydrolysis products directly at the hydrolysis site, which is energetically favorable. Furthermore, enhanced expression of genes for carbohydrate active enzymes as a response to the attachment on solid substrate has been demonstrated for cellulolytic aerobic fungi and anerobic bacteria. In natural multispecies biofilms, the vicinity of different microbial species allows the creation of efficient food webs and synergistic interactions thereby, e.g., avoiding the accumulation of inhibiting metabolites. In this review, these topics are discussed and attempts to realize the benefits of biofilms in targeted applications such as the consolidated bioprocessing of lignocellulose are highlighted.

          Key Points

          • Multispecies biofilms enable efficient lignocellulose destruction in the biosphere.

          • Cellulose degradation by anaerobic bacteria often occurs by monolayered biofilms.

          • Fungal biofilms immobilize enzymes and substrates in an external digestion system.

          • Surface attached cultures typically show higher expression of cellulolytic enzymes.

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          Most cited references76

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          Living in a fungal world: impact of fungi on soil bacterial niche development.

          The colonization of land by plants appears to have coincided with the appearance of mycorrhiza-like fungi. Over evolutionary time, fungi have maintained their prominent role in the formation of mycorrhizal associations. In addition, however, they have been able to occupy other terrestrial niches of which the decomposition of recalcitrant organic matter is perhaps the most remarkable. This implies that, in contrast to that of aquatic organic matter decomposition, bacteria have not been able to monopolize decomposition processes in terrestrial ecosystems. The emergence of fungi in terrestrial ecosystems must have had a strong impact on the evolution of terrestrial bacteria. On the one hand, potential decomposition niches, e.g. lignin degradation, have been lost for bacteria, whereas on the other hand the presence of fungi has itself created new bacterial niches. Confrontation between bacteria and fungi is ongoing, and from studying contemporary interactions, we can learn about the impact that fungi presently have, and have had in the past, on the ecology and evolution of terrestrial bacteria. In the first part of this review, the focus is on niche differentiation between soil bacteria and fungi involved in the decomposition of plant-derived organic matter. Bacteria and fungi are seen to compete for simple plant-derived substrates and have developed antagonistic strategies. For more recalcitrant organic substrates, e.g. cellulose and lignin, both competitive and mutualistic strategies appear to have evolved. In the second part of the review, bacterial niches with respect to the utilization of fungal-derived substrates are considered. Here, several lines of development can be recognized, ranging from mutualistic exudate-consuming bacteria that are associated with fungal surfaces to endosymbiotic and mycophagous bacteria. In some cases, there are indications of fungal specific selection in fungus-associated bacteria, and possible mechanisms for such selection are discussed.
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            Soil enzymes in a changing environment: Current knowledge and future directions

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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
                michael.studer1@bfh.ch
                Journal
                Appl Microbiol Biotechnol
                Appl. Microbiol. Biotechnol
                Applied Microbiology and Biotechnology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0175-7598
                1432-0614
                26 April 2020
                26 April 2020
                2020
                : 104
                : 12
                : 5201-5212
                Affiliations
                GRID grid.424060.4, ISNI 0000 0001 0688 6779, School of Agricultural, Forest and Food Sciences, Laboratory of Biofuels and Biochemicals, , Bern University of Applied Sciences (BFH), ; 3052 Zollikofen, Switzerland
                Article
                10595
                10.1007/s00253-020-10595-y
                7275028
                32337627
                372671f0-275b-4c67-a2f3-0fae8e4ca936
                © 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 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/.

                History
                : 20 December 2019
                : 24 March 2020
                : 31 March 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 407040-153868
                Funded by: FundRef http://dx.doi.org/10.13039/501100013348, Innosuisse - Schweizerische Agentur für Innovationsförderung;
                Award ID: SCCER BIOSWEET
                Categories
                Mini-Review
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2020

                Biotechnology
                biofilm,cellulose degradation,cellulolytic enzymes,solid state fermentation,microbial communities

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