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Selective Enhancement of Autotrophic Acetate Production with Genetically Modified Acetobacterium Woodii

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Selective Enhancement of Autotrophic Acetate Production with Genetically Modified Acetobacterium Woodii Journal of Biotechnology 178 (2014) 67–72 Contents lists available at ScienceDirect Journal of Biotechnology j ournal homepage: www.elsevier.com/locate/jbiotec Selective enhancement of autotrophic acetate production with genetically modified Acetobacterium woodii a,∗,1 b b a Melanie Straub , Martin Demler , Dirk Weuster-Botz , Peter Dürre a Institut für Mikrobiologie und Biotechnologie, Universität Ulm, Albert-Einstein-Allee 11, D-89081 Ulm, Germany b Lehrstuhl für Bioverfahrenstechnik, Technische Universität München, Boltzmannstr. 15, D-85748 Garching, Germany a r a t i b s c t l e i n f o r a c t Article history: Great interest has emerged in the recent past towards the potential of autotrophic acetogenic bacte- Received 13 December 2013 ria for the sustainable production of fuels and chemicals. This group of microorganisms possesses an Received in revised form 21 February 2014 ancient pathway for the fixation of carbon dioxide in the presence of hydrogen, making them highly Accepted 1 March 2014 attractive for the utilization of gas mixtures as a cheap and abundant carbon and energy source. As Available online 15 March 2014 more and more genome sequence data of acetogens becomes available, the genetic tools are being developed concomitantly. Here, we demonstrate for the first time the genetic modification of the well- Keywords: characterized acetogen Acetobacterium woodii. This microorganism selectively produces acetate under Acetate autotrophic conditions, but seems to be limited at high acetate concentrations. To increase the carbon Acetobacterium woodii Autotrophic flow through the Wood–Ljungdahl pathway and therefore increase the efficiency of CO2 fixation, genes of Genetic modification enzyme groups of this pathway were selectively overexpressed (the four THF-dependent enzymes for the CO2 + H2 processing of formate as well as phosphotransacetylase and acetate kinase to enhance an ATP-generation step). Acetate production with genetically modified strains was increased in a batch process under pH- controlled reaction conditions in a stirred-tank reactor with continuous sparging of H2 and CO2. Final −1 acetate concentrations of more than 50 g L acetate were thus measured with the recombinant strains −1 at low cell concentrations of 1.5–2 g L dry cell mass in less than four days under autotrophic conditions. © 2014 Elsevier B.V. All rights reserved. 1. Introduction If acetate is the sole end product, this way of fermentation is called homoacetogenesis. CO2, which is either produced during Acetate is a commodity chemical, which is mainly produced glycolysis in the pyruvate:ferredoxin oxidoreductase reaction or catalytically via carbonylation of methanol. It is a precursor for used directly in the autotrophic mode of metabolism, is reduced in the production of a variety of chemical products such as polyvinyl the Wood–Ljungdahl-pathway with the produced reducing equiv- 6 acetates. About 2 × 10 t acetate per year are also produced biotech- alents or hydrogen to another mol of acetate (Ragsdale and Pierce, nologically with aerobic acetic acid bacteria, e.g. Acetobacter and 2008). So, under heterotrophic conditions there is an increase of Gluconobacter, via oxidative fermentation of molasses (Steinborn, acetate production of 50% compared to the oxidative fermentation 2007). Today, biotechnologically produced acetate is used exclu- of ethanol by aerobic acetic acid bacteria, according to the equation: sively for the production of vinegar. Besides acetic acid bacteria, another group of microorganisms − + ◦ C6H12O6 → 3CH3COO + 3H G = −310.9 kJ/mol is also able to produce acetate under anaerobic conditions with syn(thesis) gas as a substrate. Some of these acetogenic bacte- 13 Globally, acetogens produce about 10 kg acetate annually ria form ethanol, butanol, butyrate, and 2,3-butanediol under (Ragsdale and Pierce, 2008). The overall autotrophic process can autotrophic conditions, in addition to the main end product acetate be described according to the equation: (Mohammadi et al., 2011; Köpke et al., 2011). − + ◦ CO2 + 4H2 → CH3COO + H + 2H2O G = −95 kJ/mol ∗ Detailed recent reviews of acetogens and their metabolic fea- Corresponding author. Tel.: +49 7351 582430; fax: +49 7351 582469. tures are given by Ragsdale and Pierce (2008) and Drake et al. E-mail address: [email protected] (M. Straub). 1 (2008). In the recent past, the interest in autotrophic produc- Present address: Institut f r Angewandte Biotechnologie, Hochschule Biberach, Hubertus-Liebrecht-Stra e 35, D-88400 Biberach, Germany. tion of solvents and acids with acetogenic bacteria increased http://dx.doi.org/10.1016/j.jbiotec.2014.03.005 0168-1656/© 2014 Elsevier B.V. All rights reserved. 68 M. Straub et al. / Journal of Biotechnology 178 (2014) 67–72 ◦ type tubes in 50% (v/v) glycerol at −80 C. A. woodii DSM1030 Nomenclature was provided from Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany. Chemically compe- ack acetate kinase tent E. coli XL1 blue MRF cells were used for all cloning experiments pCO2,in partial pressure of carbon dioxide at the inlet of the and vector maintenance. E. coli JM109 pMCljS cells were used to reactor (mbar) methylate plasmid DNA in vivo before transformation into A. woodii. pH2,in partial pressure of hydrogen at the inlet of the reac- tor (mbar) 2.2. Media and growth conditions pta phosphotransacetylase THF tetrahydrofolate E. coli strains were cultivated in lysogeny broth (Luria–Bertani) ◦ medium at 37 C. For plates, we used LB medium with agar −1 (15 g L ) (Sambrook and Russell, 2001). tremendously. This is due to the fact that more and more genome The standard medium for A. woodii contained per liter: sequence data of acetogens is becoming available. The genome NH4Cl 1.0 g: KH2PO4 0.33 g; K2HPO4 0.45 g; MgSO4 × 7H2O 0.16 g; sequences of the acetogens Moorella thermoacetica (Pierce et al., yeast extract 2.0 g (Roth Chemie GmbH, Karlsruhe, Germany); 2008), Clostridium ljungdahlii (Köpke et al., 2010, 2011), Clostridium NaHCO3 10.0 g; cysteine–HCl × H2O 0.5 g; Na2S × 9H2O 0.5 g; carboxidivorans (Bruant et al., 2010; Paul et al., 2010), and Eubac- nitrilotriacetic acid 30 mg; MnSO4 × H2O 10 mg; NaCl 20 mg; × terium limosum (Roh et al., 2010)) are published. Concomitantly, FeSO4 7H2O 2 mg; CoSO4 × 7H2O 3.6 mg; CaCl2 × 2H2O 2 mg; the development of genetic tools is picking up (Schiel-Bengelsdorf ZnSO4 × 7H2O 3.6 mg; CuSO4 × 5H2O 0.2 mg; KAI(SO4)2 × 12H2O and Dürre, 2012). The first genetically modified acetogen was C. 0.4 mg; H3BO3 0.2 mg; Na2MoO4 × 2H2O 0.2 mg; NiCl2 × 6H2O −3 −5 ljungdahlii. Both Köpke et al. (2010, 2011) and Leang et al. (2012) 0.5 mg; Na2SeO3 × 5H2O 6 × 10 mg; biotin 4 × 10 mg; folic acid −5 × suggested this microorganism as a microbial platform for the 4 10 ; pyridoxine–HCl 0.2 mg; thiamine–HC × 2H2O 0.1 mg; production of fuels and chemicals based on syngas as substrate. riboflavin 0.1 mg; nicotinic acid 0.1 mg; d-Ca–pantothenate 0.1 mg; −6 Furthermore, a genetic transformation system was developed for cyanocobalamine 2 × 10 mg; p-aminobenzoic acid 0.1 mg; lipoic the acetogen M. thermoacetica (Kita et al., 2012). acid 0.1 mg. Batch experiments were performed in 125-mL Besides M. thermoacetica and Clostridium aceticum, Acetobac- Müller–Krempel bottles (Bülach, Switzerland) filled with 50 mL ◦ terium woodii (Balch et al., 1977) has already been studied for the sterile medium at 30 C. Growth experiments on fructose con- −1 autotrophic production of acetate as well (e.g. Parekh and Cheryan, tained 10 g L fructose. Autotrophic batch experiments contained 1991; Sim and Kamaruddin, 2008; Demler and Weuster-Botz, a mixture of H2:CO2 (67:33) at atmospheric pressure. Thiampheni- 2011). A. woodii produces acetate specifically either on fructose col or clarythromycin were used as antibiotics in a concentration −1 −1 or on CO2 + H2 as carbon sources. With this microorganism, up of 25 ␮g mL or 5 ␮g mL . The 125-mL Müller–Krempel bottles −1 to 44 g L acetate could be produced with H2 + CO2 as substrates (Bülach, Switzerland) were inoculated with 10% inoculum. The in a batch-operated stirred-tank reactor by controlling the pH inoculum stemmed from a preculture, grown on the same medium. at pH 7.0 (Demler and Weuster-Botz, 2011). One possibility to overcome the decrease of acetate production of A. woodii at high 2.3. Autotrophic cultivation in a stirred-tank reactor acetate concentrations may be the enhancement of the carbon flow through the Wood–Ljungdahl pathway by overexpression For autotrophic cultivations on a liter-scale, medium with- of enzyme groups of this pathway. Peters et al. assumed that out fructose was used. Furthermore, the concentrations of yeast the processing of formate by tetrahydrofolate (THF)-dependent extract, vitamins, and trace elements were doubled to avoid any 2+ enzymes in the Wood–Ljungdahl pathway constitutes a bottleneck growth limitation. As the concentration of Fe was shown to in the catabolism of CO2 and H2 (Peters et al., 1999). have a supportive influence on growth and productivity of A. Therefore, one of our approaches to enhance acetate productiv- woodii (Demler and Weuster-Botz, submitted), the concentration 2+ −1 ity was the concomitant overexpression of the four THF-dependent of Fe was increased to 5.4 mg L . Thiamphenicol was used as −1 enzymes of this pathway. An ATP-generating step in this CO2-fixing an antibiotic in a concentration of 20 mg L . Cultivations were pathway is the conversion of acetyl-CoA to acetate that is catalyzed carried out in a 2-L stirred tank bioreactor (Labfors, Infors, Bottmin- by phosphotransacetylase and acetate kinase (Ragsdale and Pierce, gen, Switzerland) with a working volume of 1 L at a temperature ◦ 2008). Our second approach to enhance acetate productivity thus of 30 C under anaerobic conditions.
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