Abstract
A three-step biohydrogen production process characterized by efficient anaerobic induction of the formate hydrogen lyase (FHL) of aerobically grown Escherichia coli was established. Using E. coli strain SR13 (fhlA ++, ΔhycA) at a cell density of 8.2 g/l medium in this process, a specific hydrogen productivity (28.0 ± 5.0 mmol h−1 g−1 dry cell) of one order of magnitude lower than we previously reported was realized after 8 h of anaerobic incubation. The reduced productivity was attributed partly to the inhibitory effects of accumulated metabolites on FHL induction. To avoid this inhibition, strain SR14 (SR13 ΔldhA ΔfrdBC) was constructed and used to the effect that specific hydrogen productivity increased 1.3-fold to 37.4 ± 6.9 mmol h−1 g−1. Furthermore, a maximum hydrogen production rate of 144.2 mmol h−1 g−1 was realized when a metabolite excretion system that achieved a dilution rate of 2.0 h−1 was implemented. These results demonstrate that by avoiding anaerobic cultivation altogether, more economical harvesting of hydrogen-producing cells for use in our biohydrogen process was made possible.
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References
Alam KY, Clark DP (1989) Anaerobic fermentation balance of Escherichia coli as observed by in vivo nuclear magnetic resonance spectroscopy. J Bacteriol 171:6213–6217
Benemann J (1996) Hydrogen biotechnology: progress and prospects. Nat Biotechnol 14:1101–1103
Böhm R, Sauter M, Böck A (1990) Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol 4:231–243
Chin HL, Chen ZS, Chou CP (2003) Fedbatch operation using Clostridium acetobutylicum suspension culture as biocatalyst for enhancing hydrogen production. Biotechnol Prog 19:383–388
Hirshfield IN, Terzulli S, O’Byrne C (2003) Weak organic acids: a panoply of effects on bacteria. Sci Prog 86:245–269
Inui M, Kawaguchi H, Murakami S, Vertès AA, Yukawa H (2004) Metabolic engineering of Corynebacterium glutamicum for fuel ethanol production under oxygen-deprivation conditions. J Mol Microbiol Biotechnol 8:243–254
Kirkpatrick C, Maurer LM, Oyelakin NE, Yoncheva YN, Maurer R, Slonczewski JL (2001) Acetate and formate stress: opposite responses in the proteome of Escherichia coli. J Bacteriol 183:6466–6477
Kumar N, Das D (2001) Continuous hydrogen production by immobilized Enterobacter cloacae IIT-BT 08 using lignocellulosic materials as solid matrices. Enzyme Microb Technol 29:280–287
Lee KS, Wu JF, Lo YS, Lo YC, Lin PJ, Chang JS (2004) Anaerobic hydrogen production with an efficient carrier-induced granular sludge bed bioreactor. Biotechnol Bioeng 87:648–657
Leonhartsberger S, Korsa I, Böck A (2002) The molecular biology of formate metabolism in enterobacteria. J Mol Microbiol Biotechnol 4:269–276
Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748
Nandi R, Bhattacharya PK, Bhaduri AN, Sengupta S (1992) Synthesis and lysis of formate by immobilized cells of Escherichia coli. Biotechnol Bioeng 39:775–780
Presser KA, Ratkowsky DA, Ross T (1997) Modelling the growth rate of Escherichia coli as a function of pH and lactic acid concentration. Appl Environ Microbiol 63:2355–2360
Rossmann R, Sawers G, Böck A (1991) Mechanism of regulation of the formate-hydrogen lyase pathway by oxygen, nitrate, and pH: Definition of the formate regulon. Mol Microbiol 5:2807–2814
Sauter M, Böhm R, Böck A (1992) Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol 6:1523–1532
Takahashi CM, Takahashi DF, Carvalhal ML, Alterthum F (1999) Effects of acetate on the growth and fermentation performance of Escherichia coli KO11. Appl Biochem Biotechnol 81:193–203
Tsygankov AA, Hirata Y, Miyake M, Asada Y, Miyake J (1994) Photobioreactor with photosynthetic bacteria immobilized on porous glass for hydrogen photoproduction. J Ferment Bioeng 77:575–578
Van Ginkel S, Logan BE (2005) Inhibition of biohydrogen production by undissociated acetic and butyric acids. Environ Sci Technol 39:9351–9356
Yoshida A, Nishimura T, Kawaguchi H, Inui M, Yukawa H (2005) Enhanced hydrogen production from formic acid by formate hydrogen lyase-overexpressing Escherichia coli strains. Appl Environ Microbiol 71:6762–6768
Yoshida A, Nishimura T, Kawaguchi H, Inui M, Yukawa H (2006) Enhanced hydrogen production from glucose using ldh- and frd-inactivated Escherichia coli strains. Appl Microbiol Biotechnol 73:67–72
Zaldivar J, Ingram LO (1999) Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol Bioeng 66:203–210
Zheng XJ, Yu HQ (2005) Inhibitory effects of butyrate on biological hydrogen production with mixed anaerobic cultures. J Environ Manage 74:65–70
Zinoni F, Birkmann A, Stadtman TC, Böck A (1986) Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. Proc Natl Acad Sci USA 83:4650–4654
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We thank C. A. Omumasaba (Research Institute of Innovative Technology for the Earth) for helpful comments on the manuscript.
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Yoshida, A., Nishimura, T., Kawaguchi, H. et al. Efficient induction of formate hydrogen lyase of aerobically grown Escherichia coli in a three-step biohydrogen production process. Appl Microbiol Biotechnol 74, 754–760 (2007). https://doi.org/10.1007/s00253-006-0721-y
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DOI: https://doi.org/10.1007/s00253-006-0721-y