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      Whole-cell biocatalysis for hydrogen storage and syngas conversion to formate using a thermophilic acetogen

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          Abstract

          Background

          In times of global climate change, the conversion and capturing of inorganic CO 2 have gained increased attention because of its great potential as sustainable feedstock in the production of biofuels and biochemicals. CO 2 is not only the substrate for the production of value-added chemicals in CO 2-based bioprocesses, it can also be directly hydrated to formic acid, a so-called liquid organic hydrogen carrier (LOHC), by chemical and biological catalysts. Recently, a new group of enzymes were discovered in the two acetogenic bacteria Acetobacterium woodii and Thermoanaerobacter kivui which catalyze the direct hydrogenation of CO 2 to formic acid with exceptional high rates, the hydrogen-dependent CO 2 reductases (HDCRs). Since these enzymes are promising biocatalysts for the capturing of CO 2 and the storage of molecular hydrogen in form of formic acid, we designed a whole-cell approach for T. kivui to take advantage of using whole cells from a thermophilic organism as H 2/CO 2 storage platform. Additionally, T. kivui cells were used as microbial cell factories for the production of formic acid from syngas.

          Results

          This study demonstrates the efficient whole-cell biocatalysis for the conversion of H 2 + CO 2 to formic acid in the presence of bicarbonate by T. kivui. Interestingly, the addition of KHCO 3 not only stimulated formate formation dramatically but it also completely abolished unwanted side product formation (acetate) under these conditions and bicarbonate was shown to inhibit the membrane-bound ATP synthase. Cell suspensions reached specific formate production rates of 234 mmol g protein −1 h −1 (152 mmol g CDW −1 h −1), the highest rates ever reported in closed-batch conditions. The volumetric formate production rate was 270 mmol L −1 h −1 at 4 mg mL −1. Additionally, this study is the first demonstration that syngas can be converted exclusively to formate using an acetogenic bacterium and high titers up to 130 mM of formate were reached.

          Conclusions

          The thermophilic acetogenic bacterium T. kivui is an efficient biocatalyst which makes this organism a promising candidate for future biotechnological applications in hydrogen storage, CO 2 capturing and syngas conversion to formate.

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          Most cited references50

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          Clostridium ljungdahlii represents a microbial production platform based on syngas.

          Clostridium ljungdahlii is an anaerobic homoacetogen, able to ferment sugars, other organic compounds, or CO(2)/H(2) and synthesis gas (CO/H(2)). The latter feature makes it an interesting microbe for the biotech industry, as important bulk chemicals and proteins can be produced at the expense of CO(2), thus combining industrial needs with sustained reduction of CO and CO(2) in the atmosphere. Sequencing the complete genome of C. ljungdahlii revealed that it comprises 4,630,065 bp and is one of the largest clostridial genomes known to date. Experimental data and in silico comparisons revealed a third mode of anaerobic homoacetogenic metabolism. Unlike other organisms such as Moorella thermoacetica or Acetobacterium woodii, neither cytochromes nor sodium ions are involved in energy generation. Instead, an Rnf system is present, by which proton translocation can be performed. An electroporation procedure has been developed to transform the organism with plasmids bearing heterologous genes for butanol production. Successful expression of these genes could be demonstrated, leading to formation of the biofuel. Thus, C. ljungdahlii can be used as a unique microbial production platform based on synthesis gas and carbon dioxide/hydrogen mixtures.
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            Carbon dioxide and formic acid—the couple for environmental-friendly hydrogen storage?

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              Liquid Organic Hydrogen Carriers (LOHCs): Toward a Hydrogen-free Hydrogen Economy

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                Author and article information

                Contributors
                vmueller@bio.uni-frankfurt.de
                Journal
                Biotechnol Biofuels
                Biotechnol Biofuels
                Biotechnology for Biofuels
                BioMed Central (London )
                1754-6834
                28 February 2020
                28 February 2020
                2020
                : 13
                : 32
                Affiliations
                GRID grid.7839.5, ISNI 0000 0004 1936 9721, Molecular Microbiology & Bioenergetics, Institute of Molecular Biosciences, , Johann Wolfgang Goethe University, ; Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Germany
                Author information
                http://orcid.org/0000-0001-7955-5508
                Article
                1670
                10.1186/s13068-020-1670-x
                7048051
                32140177
                002921dd-4e29-4787-8aff-dce0f4ac2280
                © 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
                : 9 November 2019
                : 28 January 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007601, Horizon 2020;
                Award ID: 741791
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Biotechnology
                carbon capture,syngas,whole-cell biocatalysis,closed-batch fermentation,hydrogen-dependent co2 reductase,formate dehydrogenase,hydrogenase,thermophiles,thermoanaerobacter kivui

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