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Diversity of metabolic shift in response to oxygen deprivation in Corynebacterium glutamicum and its close relatives

  • Applied Microbial and Cell Physiology
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Abstract

Oxygen-deprived Corynebacterium glutamicum R cells remain metabolically active, producing considerable amounts of organic acids even when not actively growing. We compared the proficiencies of C. glutamicum and close relatives grown under aerobic conditions to metabolize glucose when deprived of oxygen. Eight strains that readily consumed glucose without cell growth subsequently produced organic acids. Among these, the glucose consumption rates of the two C. glutamicum strains (>40 mM/h) and Corynebacterium efficiens (>12 mM/h) were an order of magnitude higher than those of the other five strains. The resultant organic acid yields of these three strains (>86%) consequently exceeded those of the other five (<60%). This difference is probably rooted in the comparatively inferior activities of glyceraldehyde-3-phosphate dehydrogenase, lactate dehydrogenase, and malate dehydrogenase observed in the five strains. Moreover, under oxygen deprivation, phosphoenolpyruvate carboxylase (PEPC) activity of C. efficiens was elevated tenfold, but its lack of fumarase activity meant that no succinic acid could be produced. The metabolic shift occasioned by addition of the PEPC substrate sodium bicarbonate resulted in a doubling of the glucose consumption rate of the two C. glutamicum strains but not that of the other six close relatives.

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References

  • Abe S, Takayama K, Kinoshita S (1967) Taxonomical studies on glutamic acid-producing bacteria. J Gen Appl Microbiol 13:279–301

    Article  Google Scholar 

  • Barksdale L (1970) Corynebacterium diphtheriae and its relatives. Bacteriol Rev 34:378–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan BB, Pine L (1967) Path of glucose breakdown and cell yields of a facultative anaerobe, Actinomyces naeslundii. J Gen Microbiol 46:225–236

    Article  CAS  PubMed  Google Scholar 

  • Chen HH, Li WJ, Tang SK, Kroppenstedt RM, Stackebrandt E, Xu LH, Jiang CL (2004) Corynebacterium halotolerans sp. nov., isolated from saline soil in the west of China. Int J Syst Evol Microbiol 54:779–782

    Article  CAS  PubMed  Google Scholar 

  • Collins MD (1987a) Transfer of Arthrobacter variabilis (Muller) to the genus Corynebacterium, as Corynebacterium variabilis comb. nov. Int J Syst Bacteriol 37:287–288

    Article  Google Scholar 

  • Collins MD (1987b) Transfer of Brevibacterium ammoniagenes (Cooke and Keith) to the genus Corynebacterium as Corynebacterium ammoniagenes comb. nov. Int J Syst Bacteriol 37:442–443

    Article  Google Scholar 

  • Conn HJ, Dimmick I (1947) Soil bacteria similar in morphology to Mycobacterium and Corynebacterium. J Bacteriol 54:291–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooke JV, Keith HR (1927) A type of urea-splitting bacterium found in the human intestinal tract. J Bacteriol 13:315–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fudou R, Jojima Y, Seto A, Yamada K, Kimura E, Nakamatsu T, Hiraishi A, Yamanaka S (2002) Corynebacterium efficiens sp. nov., a glutamic-acid-producing species from soil and vegetables. Int J Syst Evol Microbiol 52:1127–1131

    CAS  PubMed  Google Scholar 

  • Harper C, Hayward D, Wiid I, van Helden P (2008) Regulation of nitrogen metabolism in Mycobacterium tuberculosis: a comparison with mechanisms in Corynebacterium glutamicum and Streptomyces coelicolor. IUBMB Life 60:643–650

    Article  CAS  PubMed  Google Scholar 

  • Ikeda M, Nakagawa S (2003) The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol 62:99–109

    Article  CAS  PubMed  Google Scholar 

  • Inui M, Kawaguchi H, Murakami S, Vertès AA, Yukawa H (2004a) Metabolic engineering of Corynebacterium glutamicum for fuel ethanol production under oxygen-deprivation conditions. J Mol Microbiol Biotechnol 8:243–254

    Article  CAS  PubMed  Google Scholar 

  • Inui M, Murakami S, Okino S, Kawaguchi H, Vertès AA, Yukawa H (2004b) Metabolic analysis of Corynebacterium glutamicum during lactate and succinate productions under oxygen deprivation conditions. J Mol Microbiol Biotechnol 7:182–196

    Article  CAS  PubMed  Google Scholar 

  • Inui M, Suda M, Okino S, Nonaka H, Puskás LG, Vertès AA, Yukawa H (2007) Transcriptional profiling of Corynebacterium glutamicum metabolism during organic acid production under oxygen deprivation conditions. Microbiology 153:2491–2504

    Article  CAS  PubMed  Google Scholar 

  • Jones AL, Koerner RJ, Natarajan S, Perry JD, Goodfellow M (2008) Dietzia papillomatosis sp. nov., a novel actinomycete isolated from the skin of an immunocompetent patient with confluent and reticulated papillomatosis. Int J Syst Evol Microbiol 58:68–72

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, Goesmann A, Hartmann M, Huthmacher K, Krämer R, Linke B, McHardy AC, Meyer F, Möckel B, Pfefferle W, Pühler A, Rey DA, Rückert C, Rupp O, Sahm H, Wendisch VF, Wiegräbe I, Tauch A (2003) The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of l-aspartate-derived amino acids and vitamins. J Biotechnol 104:5–25

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P, Andersson MA, Rainey FA, Kroppenstedt RM, Salkinoja-Salonen M (1999) Williamsia muralis gen. nov., sp. nov., isolated from the indoor environment of a children’s day care centre. Int J Syst Bacteriol 49:681–687

    Article  PubMed  Google Scholar 

  • Kikuchi M, Nakao Y (1973) Relation between cellular phospholipids and the excretion of l-glutamic acid by a glycerol auxotroph of Corynebacterium alkanolyticum. Agric Biol Chem 37:515–519

    Article  CAS  Google Scholar 

  • Kinoshita S (1985) Glutamic acid bacteria. In: Demain L, Solomon NA (eds) Biology of industrial microorganisms. Benjamin Cummings, London, pp 115–146

    Google Scholar 

  • Kinoshita S, Nakayama K, Akita S (1958) Taxonomical study of glutamic acid accumulating bacteria, Micrococcus glutamicus nov. sp. Bull Agric Chem Soc Jpn 22:176–185

    Google Scholar 

  • Klatte S, Kroppenstedt RM, Rainey FA (1994) Rhodococcus opacus sp. nov., an unusual nutritionally versatile Rhodococcus-species. Syst Appl Microbiol 17:355–360

    Article  Google Scholar 

  • Krawczyk J, Kohl TA, Goesmann A, Kalinowski J, Baumbach J (2009) From Corynebacterium glutamicum to Mycobacterium tuberculosis—towards transfers of gene regulatory networks and integrated data analyses with MycoRegNet. Nucleic Acids Res 37:e97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kurusu Y, Satoh Y, Inui M, Kohama K, Kobayashi M, Terasawa M, Yukawa H (1991) Identification of plasmid partition function in Coryneform bacteria. Appl Environ Microbiol 57:759–764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanéelle MA, Asselineau J, Welby M, Norgard MV, Imaeda T, Pollice MC, Barksdale L (1980) Biological and chemical bases for the reclassification of Brevibacterium vitarumen (Bechdel et al.) breed (approved lists, 1980) as Corynebacterium vitarumen (Bechdel et al.) comb. nov. and Brevibacterium liquefaciens Okabayashi and Masuo (approved lists, 1980) as Corynebacterium liquefaciens (Okabayashi and Masuo) comb. nov. Int J Syst Bacteriol 30:539–546

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Liebl W, Ehrmann M, Ludwig W, Schleifer KH (1991) Transfer of Brevibacterium divaricatum DSM 20297T, "Brevibacterium flavum" DSM 20411, "Brevibacterium lactofermentum" DSM 20412 and DSM 1412, and Corynebacterium glutamicum and their distinction by rRNA gene restriction patterns. Int J Syst Bacteriol 41:255–260

    Article  CAS  PubMed  Google Scholar 

  • Lozada-Ramírez JD, Martínez-Martínez I, García-Carmona F, Sánchez-Ferrer A (2008) Cloning, overexpression, purification, and characterization of S-adenosylhomocysteine hydrolase from Corynebacterium efficiens YS-314. Biotechnol Prog 24:120–127

    Article  PubMed  CAS  Google Scholar 

  • Nakano MM, Zuber P (1998) Anaerobic growth of a "strict aerobe" (Bacillus subtilis). Annu Rev Microbiol 52:165–190

    Article  CAS  PubMed  Google Scholar 

  • Nakayama K, Kitada S, Kinoshita S (1961) Studies on lysine fermentation I. The control mechanism on lysine accumulation by homoserine and threonine. J Gen Appl Microbiol 7:145–154

    Article  CAS  Google Scholar 

  • Nam SW, Chun J, Kim S, Kim W, Zakrzewska-Czerwinska J, Goodfellow M (2003) Tsukamurella spumae sp. nov., a novel actinomycete associated with foaming in activated sludge plants. Syst Appl Microbiol 26:367–375

    Article  CAS  PubMed  Google Scholar 

  • Neuweger H, Persicke M, Albaum SP, Bekel T, Dondrup M, Hüser AT, Winnebald J, Schneider J, Kalinowski J, Goesmann A (2009) Visualizing post genomics data-sets on customized pathway maps by ProMeTra-aeration-dependent gene expression and metabolism of Corynebacterium glutamicum as an example. BMC Syst Biol 3:82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishimura T, Vertès AA, Shinoda Y, Inui M, Yukawa H (2007) Anaerobic growth of Corynebacterium glutamicum using nitrate as a terminal electron acceptor. Appl Microbiol Biotechnol 75:889–897

    Article  CAS  PubMed  Google Scholar 

  • Nishio Y, Nakamura Y, Kawarabayasi Y, Usuda Y, Kimura E, Sugimoto S, Matsui K, Yamagishi A, Kikuchi H, Ikeo K, Gojobori T (2003) Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res 13:1572–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishio Y, Nakamura Y, Usuda Y, Sugimoto S, Matsui K, Kawarabayasi Y, Kikuchi H, Gojobori T, Ikeo K (2004) Evolutionary process of amino acid biosynthesis in Corynebacterium at the whole genome level. Mol Biol Evol 21:1683–1691

    Article  CAS  PubMed  Google Scholar 

  • Oberreuter H, Charzinski J, Scherer S (2002) Intraspecific diversity of Brevibacterium linens, Corynebacterium glutamicum and Rhodococcus erythropolis based on partial 16S rDNA sequence analysis and Fourier-transform infrared (FT-IR) spectroscopy. Microbiology 148:1523–1532

    Article  CAS  PubMed  Google Scholar 

  • Okino S, Inui M, Yukawa H (2005) Production of organic acids by Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 68:475–480

    Article  CAS  PubMed  Google Scholar 

  • Okino S, Noburyu R, Suda M, Jojima T, Inui M, Yukawa H (2008a) An efficient succinic acid production process in a metabolically engineered Corynebacterium glutamicum strain. Appl Microbiol Biotechnol 81:459–464

    Article  CAS  PubMed  Google Scholar 

  • Okino S, Suda M, Fujikura K, Inui M, Yukawa H (2008b) Production of d-lactic acid by Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 78:449–454

    Article  CAS  PubMed  Google Scholar 

  • Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369

    Article  CAS  PubMed  Google Scholar 

  • Portevin D, De Sousa-D’Auria C, Houssin C, Grimaldi C, Chami M, Daffé M, Guilhot C (2004) A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci USA 101:314–319

    Article  CAS  PubMed  Google Scholar 

  • Sacchettini JC, Meininger T, Roderick S, Banaszak LJ (1986) Purification, crystallization, and preliminary X-ray data for porcine fumarase. J Biol Chem 261:15183–15185

    CAS  PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schramm G, Zapatka M, Eils R, König R (2007) Using gene expression data and network topology to detect substantial pathways, clusters and switches during oxygen deprivation of Escherichia coli. BMC Bioinform 8:149

    Article  CAS  Google Scholar 

  • Seidel M, Alderwick LJ, Sahm H, Besra GS, Eggeling L (2007) Topology and mutational analysis of the single Emb arabinofuranosyltransferase of Corynebacterium glutamicum as a model of Emb proteins of Mycobacterium tuberculosis. Glycobiology 17:210–219

    Article  CAS  PubMed  Google Scholar 

  • Shirai T, Nakato A, Izutani N, Nagahisa K, Shioya S, Kimura E, Kawarabayasi Y, Yamagishi A, Gojobori T, Shimizu H (2005) Comparative study of flux redistribution of metabolic pathway in glutamate production by two coryneform bacteria. Metab Eng 7:59–69

    Article  CAS  PubMed  Google Scholar 

  • Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WR Jr (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4:1911–1919

    Article  CAS  PubMed  Google Scholar 

  • Soddell JA, Stainsby FM, Eales KL, Kroppenstedt RM, Seviour RJ, Goodfellow M (2006) Millisia brevis gen. nov., sp. nov., an actinomycete isolated from activated sludge foam. Int J Syst Evol Microbiol 56:739–744

    Article  CAS  PubMed  Google Scholar 

  • Takahashi N, Yamada T (1992) Stimulatory effect of bicarbonate on the glycolysis of Actinomyces viscosus and its biochemical mechanism. Oral Microbiol Immunol 7:165–170

    Article  CAS  PubMed  Google Scholar 

  • Takahashi N, Yamada T (1999a) Effects of pH on the glucose and lactate metabolisms by the washed cells of Actinomyces naeslundii under anaerobic and aerobic conditions. Oral Microbiol Immunol 14:60–65

    Article  CAS  PubMed  Google Scholar 

  • Takahashi N, Yamada T (1999b) Glucose and lactate metabolism by Actinomyces naeslundii. Crit Rev Oral Biol Med 10:487–503

    Article  CAS  PubMed  Google Scholar 

  • Takahashi N, Kalfas S, Yamada T (1994) The role of the succinate pathway in sorbitol fermentation by oral Actinomyces viscosus and Actinomyces naeslundii. Oral Microbiol Immunol 9:218–223

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi M, Sakane T, Nihira T, Yamada Y, Imai K (1999) Corynebacterium terpenotabidum sp. nov., a bacterium capable of degrading squalene. Int J Syst Bacteriol 49:223–229

    Article  CAS  PubMed  Google Scholar 

  • Terasawa M, Yukawa H (1993) Industrial production of biochemicals by native immobilization. Bioprocess Technol 16:37–52

    CAS  PubMed  Google Scholar 

  • Walter B, Hänssler E, Kalinowski J, Burkovski A (2007) Nitrogen metabolism and nitrogen control in corynebacteria: variations of a common theme. J Mol Microbiol Biotechnol 12:131–138

    Article  CAS  PubMed  Google Scholar 

  • Yassin AF, Hupfer H (2006) Williamsia deligens sp. nov., isolated from human blood. Int J Syst Evol Microbiol 56:193–197

    Article  CAS  PubMed  Google Scholar 

  • Yassin AF, Rainey FA, Burghardt J, Brzezinka H, Schmitt S, Seifert P, Zimmermann O, Mauch H, Gierth D, Lux I, Schaal KP (1997) Tsukamurella tyrosinosolvens sp. nov. Int J Syst Bacteriol 47:607–614

    Article  CAS  PubMed  Google Scholar 

  • Yukawa H, Omumasaba CA, Nonaka H, Kós P, Okai N, Suzuki N, Suda M, Tsuge Y, Watanabe J, Ikeda Y, Vertès AA, Inui M (2007) Comparative analysis of the Corynebacterium glutamicum group and complete genome sequence of strain R. Microbiology 153:1042–1058

    Article  CAS  PubMed  Google Scholar 

  • Yumoto I, Nakamura A, Iwata H, Kojima K, Kusumoto K, Nodasaka Y, Matsuyama H (2002) Dietzia psychralcaliphila sp. nov., a novel, facultatively psychrophilic alkaliphile that grows on hydrocarbons. Int J Syst Evol Microbiol 52:85–90

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Zhang CT (2005) Genomic islands in the Corynebacterium efficiens genome. Appl Environ Microbiol 71:3126–3130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffé M (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 190:5672–5680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Crispinus A. Omumasaba (RITE) for critical reading of the manuscript. This work was partially supported by a grant from the New Energy and Industrial Technology Development Organization, Japan.

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  1. Research Institute of Innovative Technology for the Earth (RITE), 9-2, Kizugawadai, Kizugawa-shi, Kyoto, 619-0292, Japan

    Shogo Yamamoto, Masayuki Sakai, Masayuki Inui & Hideaki Yukawa

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  1. Shogo Yamamoto
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  2. Masayuki Sakai
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  3. Masayuki Inui
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Correspondence to Hideaki Yukawa.

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Yamamoto, S., Sakai, M., Inui, M. et al. Diversity of metabolic shift in response to oxygen deprivation in Corynebacterium glutamicum and its close relatives. Appl Microbiol Biotechnol 90, 1051–1061 (2011). https://doi.org/10.1007/s00253-011-3144-3

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