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Industrial robustness linked to the gluconolactonase from Zymomonas mobilis

Applied Microbiology and Biotechnology volume 101, pages 5089–5099 (2017)Cite this article

Abstract

The physiological characteristics and the potential gluconolactone production of the gluconolactonase-deficient strain, Zymomonas mobilis ZM4 gnlΔ, were investigated via growth inhibitory assay and biotransformation of glucose and fructose into gluconolactone and sorbitol, respectively. The results of ethanol fermentation studies performed in the presence of high concentration of glucose (>200 g l−1) under fermentative or aerobic conditions indicated that a significant reduction of volumetric ethanol productivity from the strain of ZM4 gnlΔ was noticeable due to the reduced rates of specific growth, sugar uptake, and biomass yield as compared with those of the parental strain ZM4. The biotransformation prepared at pH 6.0 using the permeabilized cell indicated that gluconic acid from ZM4 gnlΔ was still produced as a major product (67 g l−1) together with sorbitol (65 g l−1) rather than gluconolactone after 24 h. Only small amount of gluconolactone was transiently overproduced up to 9 g l−1, but at the end of biotransformation, all gluconolactone were oxidized into gluconic acid. This indicated that autolysis of gluconolactone at the pH led to such results despite under gluconolactonase inactivation conditions. The physiological characteristics of ZM4 gnlΔ was further investigated under various stress conditions, including suboptimal pH (3.5~6.0), temperature (25~40 °C), and presence of growth inhibitory molecules including hydrogen peroxide, ethanol, acetic acid, furfural, and so forth. The results indicated that ZM4 gnlΔ was more susceptible at high glucose concentration, low pH of 3.5, and high temperature of 40 °C and in the presence of 4 mM H2O2 comparing with ZM4. Therefore, the results were evident that gluconolactonase in Z. mobilis contributed to industrial robustness and anti-stress regulation.

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References

  • Balodite E, Strazdina I, Galinina N, McLean S, Rutkis R, Poole RK, Kalnenieks U (2014) Structure of the Zymomonas mobilis respiratory chain: oxygen affinity of electron transport and the role of cytochrome c peroxidase. Microbiology 160(9):2045–2052

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Chun U, Rogers P (1988) The simultaneous production of sorbitol from fructose and gluconic acid from glucose using an oxidoreductase of Zymomonas mobilis. Appl Microbiol Biotechnol 29(1):19–24

    CAS  Article  Google Scholar 

  • Erzinger GS, Vitolo M (2006) Zymomonas mobilis as catalyst for the biotechnological production of sorbitol and gluconic acid. Appl Biochem Biotechnol 131(1–3):787–794

    PubMed  Google Scholar 

  • Furusawa H, Sato Y, Tanaka Y, Inai Y, Amano A, Iwama M, Kondo Y, Handa S, Murata A, Nishikimi M, Goto S, Maruyama N, Takahashi R, Ishigami A (2008) Vitamin C is not essential for carnitine biosynthesis in vivo: verification in vitamin C-depleted senescence marker protein-30/gluconolactonase knockout mice. Biol Pharm Bull 31(9):1673–1679

    CAS  Article  PubMed  Google Scholar 

  • Goodman AE, Rogers PL, Skotnicki ML (1982) Minimal medium for isolation of auxotrophic Zymomonas mutants. Appl Environ Microbiol 44(2):496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa G, Yamasaki M, Kadono M, Tanaka M, Asano M, Senmaru T, Kondo Y, Fukui M, Obayashi H, Maruyama N, Nakamura N, Ishigami A (2010) Senescence marker protein-30/gluconolactonase deletion worsens glucose tolerance through impairment of acute insulin secretion. Endocrinology 151(2):529–536

    CAS  Article  PubMed  Google Scholar 

  • He MX, Wu B, Qin H, Ruan ZY, Tan FR, Wang JL, Shui ZX, Dai LC, Zhu QL, Pan K (2014) Zymomonas mobilis: a novel platform for future biorefineries. Biotechnol Biofuels 7(1):1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hucho F, Wallenfels K (1972) Glucono-δ-lactonase from Escherichia coli. Biochim Biophys Acta Enzymol 276(1):176–179

    CAS  Article  Google Scholar 

  • Invitrogen (2007) BL21(DE3)pLysS Cells. Publisher. https://catalog.invitrogen.com/index.cfm?fuseaction=viewCatalog.viewProductDetails&productDescription=597

  • Jeon YJ, Svenson CJ, Joachimsthal EL, Rogers PL (2002) Kinetic analysis of ethanol production by an acetate-resistant strain of recombinant Zymomonas mobilis. Biotechnol Lett 24(10):819–824

    CAS  Article  Google Scholar 

  • Joachimsthal E, Haggett KD, Jang J-H, Rogers PL (1998) A mutant of Zymomonas mobilis ZM4 capable of ethanol production from glucose in the presence of high acetate concentrations. Biotechnol Lett 20(2):137–142

    CAS  Article  Google Scholar 

  • Kanagasundaram V, Scopes R (1992) Isolation and characterization of the gene encoding gluconolactonase from Zymomonas mobilis. Biochim Biophys Acta 1171(2):198–200

    CAS  Article  PubMed  Google Scholar 

  • Kerr AL, Jeon YJ, Svenson CJ, Rogers PL, Neilan BA (2011) DNA restriction-modification systems in the ethanologen, Zymomonas mobilis ZM4. Appl Microbiol Biotechnol 89(3):761–769

    CAS  Article  PubMed  Google Scholar 

  • Kim IS, Barrow KD, Rogers PL (2000) Kinetic and nuclear magnetic resonance studies of xylose metabolism by recombinant Zymomonas mobilis ZM4(pZB5). Appl Environ Microbiol 66(1):186–193

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • King FG, Hossain MA (1982) The effect of temperature, pH, and initial glucose concentration on the kinetics of ethanol production by Zymomonas mobilis in batch fermentation. Biotechnol Lett 4(8):531–536

    CAS  Article  Google Scholar 

  • Kondo Y, Inai Y, Sato Y, Handa S, Kubo S, Shimokado K, Goto S, Nishikimi M, Maruyama N, Ishigami A (2006) Senescence marker protein 30 functions as gluconolactonase in L-ascorbic acid biosynthesis, and its knockout mice are prone to scurvy. Pro Natl Acad Sci 103(15):5723–5728

    CAS  Article  Google Scholar 

  • Luria SE, Delbruck M (1943) Mutation of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma K, Ruan Z, Shui Z, Wang Y, Hu G, He M (2016) Open fermentative production of fuel ethanol from food waste by an acid-tolerant mutant strain of Zymomonas mobilis. Bioresour Technol 203:295–302

    CAS  Article  PubMed  Google Scholar 

  • Neilan BA, Jacobs D, Del Dot T, Blackall LL, Hawkins PR, Cox PT, Goodman AE (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int J Syst Bacteriol 47(3):693–697

    CAS  Article  PubMed  Google Scholar 

  • Nidetzky B, Furlinger M, Gollhofer D, Haug I, Haltrich D, Kulbe KD (1997) Simultaneous enzymatic synthesis of gluconic acid and sorbitol: production, purification, and application of glucose-fructose oxidoreductase and gluconolactonase. Appl Biochem Biotechnol 63-65:173–188

    CAS  Article  PubMed  Google Scholar 

  • Parke SA, Birch GG, MacDougall DB, Stevens DA (1997) Tastes, structure and solution properties of D-glucono-1, 5-lactone. Chem Senses 22(1):53–65

    CAS  Article  PubMed  Google Scholar 

  • Promega (2007) Technical Manual: pGEM®-T and pGEM®-T Easy Vector Systems. Publisher. http://www.promega.com/tbs/tm042/tm042.pdf

  • Rogers P, Lee KJ, Tribe D (1979) Kinetics of alcohol production by Zymomonas mobilis at high sugar concentrations. Biotechnol Lett 1(4):165–170

    CAS  Article  Google Scholar 

  • Rogers PL, Lee JS, Skotnicki ML, Tribe DE (1982) Ethanol production by Zymomonas mobilis. Adv Biochem Eng 23:37–84

    Google Scholar 

  • Rogers P, Jeon Y, Lee K, Lawford H (2007) Zymomonas mobilis for fuel ethanol and higher value products biofuels. Adv Biochem Eng Biotechnol 108:263–288

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, vol 2. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sato Y, Amano A, Kishimoto Y, Takahashi K, Handa S, Maruyama N, Ishigami A (2014) Ascorbic acid prevents protein oxidation in livers of senescence marker protein-30/gluconolactonase knockout mice. Geriatr Gerontol Int 14(4):989–995

    Article  PubMed  Google Scholar 

  • Senmaru T, Yamazaki M, Okada H, Asano M, Fukui M, Nakamura N, Obayashi H, Kondo Y, Maruyama N, Ishigami A, Hasegawa G (2012) Pancreatic insulin release in vitamin C-deficient senescence marker protein-30/gluconolactonase knockout mice. J Clin Biochem Nutr 50(2):114–118

    CAS  Article  PubMed  Google Scholar 

  • Seo JS, Chong H, Park HS, Yoon KO, Jung C, Kim JJ, Hong JH, Kim H, Kim JH, Kil JI (2005) The genome sequence of the ethanologenic bacterium Zymomonas mobilis ZM4. Nat Biotechnol 23(1):63–68

    CAS  Article  PubMed  Google Scholar 

  • Shvinka JE, Pankova LM, Mežbårde IN, Licis LJ (1989) Hydrogen peroxide production by Zymomonas mobilis. Appl Microbiol Biotechnol 31(3):240–245

    Article  Google Scholar 

  • Silveira M, Jonas R (2002) The biotechnological production of sorbitol. Appl Microbiol Biotechnol 59(4–5):400–408

    CAS  PubMed  Google Scholar 

  • Strazdina I, Kravale Z, Galinina N, Rutkis R, Poole RK, Kalnenieks U (2012) Electron transport and oxidative stress in Zymomonas mobilis respiratory mutants. Arch Microbiol 194(6):461–471

    CAS  Article  PubMed  Google Scholar 

  • Wilson K (1987) Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol 2.4. 1–2.4. 5

  • Yang WB, Patil SS, Tsai CH, Lin CH, Fang JM (2002) The synthesis of L-gulose and L-xylose from δ-gluconolactone. Tetrahedron 58(2):253–259

    CAS  Article  Google Scholar 

  • Yang S, Tschaplinski TJ, Engle NL, Carroll SL, Martin SL, Davison BH, Palumbo AV, Rodriguez M, Brown SD (2009) Transcriptomic and metabolomic profiling of Zymomonas mobilis during aerobic and anaerobic fermentations. BMC Genomics 10(1):1–16

    CAS  Article  Google Scholar 

  • Yang S, Fei Q, Zhang Y, Contreras LM, Utturkar SM, Brown SD, Himmel ME, Zhang M (2016) Zymomonas mobilis as a model system for production of biofuels and biochemicals. Microb Biotechnol 9(6):699–717

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Affiliations

  1. School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Kensington, 2052, Australia

    Alfonsus Alvin, Brett A. Neilan & Young Jae Jeon

  2. Department of Microbiology, Pukyong National University, Busan, 608-737, Republic of Korea

    Junhyun Kim & Young Jae Jeon

  3. Department of Biotechnology, Pukyong National University, Busan, 608-737, Republic of Korea

    Gwi-Taek Jeong

  4. Department of Science and Environmental Studies, The Education University of Hong Kong, Tai Po, New Territories, Hong Kong

    Yiu Fai Tsang

  5. Department of Environment and Energy, Sejong University, Seoul, 143-747, Republic of Korea

    Eilhann E. Kwon

  6. School of Environmental and Life Science, The University of Newcastle, Newcastle, Australia

    Brett A. Neilan

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  1. Alfonsus Alvin
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  2. Junhyun Kim
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  3. Gwi-Taek Jeong
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  4. Yiu Fai Tsang
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  5. Eilhann E. Kwon
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  6. Brett A. Neilan
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  7. Young Jae Jeon
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Correspondence to Young Jae Jeon.

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This research as carried out with support of the National Research Foundation of Korea (NRF) under Grant No. NRF-2015R1D1A1A01056794.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Alvin, A., Kim, J., Jeong, GT. et al. Industrial robustness linked to the gluconolactonase from Zymomonas mobilis . Appl Microbiol Biotechnol 101, 5089–5099 (2017). https://doi.org/10.1007/s00253-017-8248-y

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  • DOI: https://doi.org/10.1007/s00253-017-8248-y

Keywords

  • Gene knockout
  • Gluconolactone
  • Gluconolactonase-deficient strain
  • Zymomonas mobilis
  • Robustness
  • Stress response