Skip to main content
SpringerLink
Log in

Corynebacterium glutamicum mechanosensitive channels: towards unpuzzling “glutamate efflux” for amino acid production

  • Review
  • Published:
Biophysical Reviews Aims and scope Submit manuscript

Abstract

Corynebacterium glutamicum has been utilized for industrial amino acid production, especially for monosodium glutamate (MSG), the food-additive for the “UMAMI” category of taste sensation, which is one of the five human basic tastes. Glutamate export from these cells is facilitated by the opening of mechanosensitive channels in the cell membrane within the bacterial cell envelope following specific treatments, such as biotin limitation, addition of Tween 40 or penicillin. A long-unsolved puzzle still remains how and why C. glutamicum mechanosensitive channels are activated by these treatments to export glutamate. Unlike mechanosensitive channels in other bacteria, these channels are not simply osmotic safety valves that prevent these bacteria from bursting upon a hypo-osmotic shock. They also function as metabolic valves to continuously release glutamate as components of a pump-and-leak mechanism regulating the cellular turgor pressure. Recent studies have demonstrated that the opening of the mechanosensitive channel, MscCG, mainly facilitates the efflux of glutamate and not of other amino acids and that the “force-from-lipids” gating mechanism of channels also applies to the MscCG channel. The bacterial types of mechanosensitive channels are found in cell-walled organisms from bacteria to land plants, where their physiological functions have been specialized beyond their basic function in bacterial osmoregulation. In the case of the C. glutamicum MscCG channels, they have evolved to function as specialized glutamate exporters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anishkin A, Kamaraju K, Sukharev S (2008) Mechanosensitive channel MscS in the open state: modeling of the transition, explicit simulations, and experimental measurements of conductance. J Gen Physiol 132(1):67–83

    Article  CAS  Google Scholar 

  • Bass RB, Strop P, Barclay M, Rees DC (2002) Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298(5598):1582–1587

    Article  CAS  Google Scholar 

  • Bavi N et al (2014) Biophysical implications of lipid bilayer rheometry for mechanosensitive channels. Proc Natl Acad Sci U S A 111(38):13864–13869

    Article  CAS  Google Scholar 

  • Bavi N et al (2016) The role of MscL amphipathic N terminus indicates a blueprint for bilayer mediated gating of mechanosensitive channels. Nat Commun 7:11984

    Article  CAS  Google Scholar 

  • Becker M, Krämer R (2015) MscCG from Corynebacterium glutamicum: functional significance of the C-terminal domain. Eur Biophys J 44(7):577–588

    Article  CAS  Google Scholar 

  • Becker M et al (2013) Glutamate efflux mediated by Corynebacterium glutamicum MscCG, Escherichia coli MscS, and their derivatives. Biochim Biophys Acta 1828(4):1230–1240

    Article  CAS  Google Scholar 

  • Bialecka-Fornal M, Lee HJ, Phillips R (2015) The rate of osmotic downshock determines the survival probability of bacterial mechanosensitive channel mutants. J Bacteriol 197(1):231–237

    Article  Google Scholar 

  • Börngen K et al (2010) The properties and contribution of the Corynebacterium glutamicum MscS variant to fine-tuning of osmotic adaptation. Biochim Biophys Acta 1798(11):2141–2149

    Article  Google Scholar 

  • Cantor RS (1999) Lipid composition and the lateral pressure profile in bilayers. Biophys J 76(5):2625–2639

    Article  CAS  Google Scholar 

  • Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC (1998) Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282(5397):2220–2226

    Article  CAS  Google Scholar 

  • Cox CD, Bavi N, Martinac B (2018) Bacterial Mechanosensors. Annu Rev Physiol 80:71–93

    Article  CAS  Google Scholar 

  • Hamilton ES, Haswell ES (2017) The tension-sensitive ion transport activity of MSL8 is critical for its function in pollen hydration and germination. Plant Cell Physiol 58(7):1222–1237

    Article  CAS  Google Scholar 

  • Hasegawa T, Hashimoto K-I, Kawasaki H, Nakamatsu T (2008) Changes in enzyme activities at the pyruvate node in glutamate-overproducing Corynebacterium glutamicum. J Biosci Bioeng 105(1):12–19

    Article  CAS  Google Scholar 

  • Hashimoto K et al (2010) The protein encoded by NCgl1221 in Corynebacterium glutamicum functions as a mechanosensitive channel. Biosci Biotechnol Biochem 74(12):2546–2549

    Article  CAS  Google Scholar 

  • Hashimoto K et al (2012) Glutamate is excreted across the cytoplasmic membrane through the NCgl1221 channel of Corynebacterium glutamicum by passive diffusion. Biosci Biotechnol Biochem 31 76(7):1422–1424

    Article  CAS  Google Scholar 

  • Haswell ES, Meyerowitz EM (2006) MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 16(1):1–11

    Article  CAS  Google Scholar 

  • Haswell ES, Peyronnet R, Barbier-Brygoo H, Meyerowitz EM, Frachisse JM (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr Biol 18(10):730–734

    Article  CAS  Google Scholar 

  • Hirasawa T, Saito M, Yoshikawa K, Furusawa C, Shmizu H (2018) Integrated analysis of the transcriptome and metabolome of Corynebacterium glutamicum during penicillin-induced glutamic acid production. Biotechnol J 13(5):e1700612

    Article  Google Scholar 

  • Hoischen C, Krämer R (1990) Membrane alteration is necessary but not sufficient for effective glutamate secretion in Corynebacterium glutamicum. J Bacteriol 172(6):3409–3416

    Article  CAS  Google Scholar 

  • Kawahara Y, Takahashi-Fuke K, Shimizu E, Nakamatsu T, Nakamori S (1997) Relationship between the glutamate production and the activity of 2-oxoglutarate dehydrogenase in Brevibacterium lactofermentum. Biosci Biotechnol Biochem 61(7):1109–1112

    Article  CAS  Google Scholar 

  • Kimura E, Abe C, Kawahara Y, Nakamatsu T (1996) Molecular cloning of a novel gene, dtsR, which rescues the detergent sensitivity of a mutant derived from Brevibacterium lactofermentum. Biosci Biotechnol Biochem 60(10):1565–1570

    Article  CAS  Google Scholar 

  • Kimura E, Abe C, Kawahara Y, Nakamatsu T, Tokuda H (1997) A dtsR gene-disrupted mutant of Brevibacterium lactofermentum requires fatty acids for growth and efficiently produces L-glutamate in the presence of an excess of biotin. Biochem Biophys Res Commun 234(1):157–161

    Article  CAS  Google Scholar 

  • Kimura E et al (1999) Glutamate overproduction in Corynebacterium glutamicum triggered by a decrease in the level of a complex comprising DtsR and a biotin-containing subunit. Biosci Biotechnol Biochem 63(7):1274–1278

    Article  CAS  Google Scholar 

  • Kinoshita S, Udaka S, Shimono M (1957) Studies on the amino acid fermentation on the various microorganism. J Gen Appl Microbiol 3(3):193–205

    Article  CAS  Google Scholar 

  • Krämer R (2009) Osmosensing and osmosignaling in Corynebacterium glutamicum. Amino Acids 37(3):487–497

    Article  Google Scholar 

  • Laneelle MA, Tropis M, Daffe M (2013) Current knowledge on mycolic acids in Corynebacterium glutamicum and their relevance for biotechnological processes. Appl Microbiol Biotechnol 97(23):9923–9930

    Article  CAS  Google Scholar 

  • Levina N, Totemeyer S, Stokes NR, Louis P, Jones MA, Booth IR (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18(7):1730–1737

    Article  CAS  Google Scholar 

  • Malcolm HR, Maurer JA (2012) The mechanosensitive channel of small conductance (MscS) superfamily: not just mechanosensitive channels anymore. Chembiochem 13(14):2037–2043

    Article  CAS  Google Scholar 

  • Malcolm HR, Blount P, Maurer JA (2015) The mechanosensitive channel of small conductance (MscS) functions as a Jack-in-the box. Biochim Biophys Acta 1848:159–166

    Article  CAS  Google Scholar 

  • Martinac B, Buechner M, Delcour AH, Adler J, Kung C (1987) Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci U S A 84(8):2297–2301

    Article  CAS  Google Scholar 

  • Martinac B, Adler J, & Kung C (1990) Mechanosensitive ion channels of E. coli activated by amphipaths Nature 348(6298):261–263

    Article  CAS  Google Scholar 

  • Martinac B et al (2010) Studying mechanosensitive ion channels using liposomes. Methods Mol Biol 606:31–53

    Article  CAS  Google Scholar 

  • Martinac B, Rohde PR, Cranfield CG, Nomura T (2013) Patch clamp electrophysiology for the study of bacterial ion channels in giant spheroplasts of E. coli. Methods Mol Biol 966:367–380

    Article  CAS  Google Scholar 

  • Martinac AD, Bavi N, Bavi O, Martinac B (2017) Pulling MscL open via N-terminal and TM1 helices: a computational study towards engineering an MscL nanovalve. PLoS One 12(8):e0183822

    Article  Google Scholar 

  • Murthy SE, Dubin AE, Patapoutian A (2017) Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat Rev Mol Cell Biol 18(12):771–783

    Article  CAS  Google Scholar 

  • Nakamura J, Hirano S, Ito H, Wachi M (2007) Mutations of the Corynebacterium glutamicum NCgl1221 gene, encoding a mechanosensitive channel homolog, induce L-glutamic acid production. Appl Environ Microbiol 73(14):4491–4498

    Article  CAS  Google Scholar 

  • Nakayama Y, Fujiu K, Sokabe M, Yoshimura K (2007) Molecular and electrophysiological characterization of a mechanosensitive channel expressed in the chloroplasts of Chlamydomonas. Proc Natl Acad Sci U S A 104(14):5883–5888

    Article  CAS  Google Scholar 

  • Nakayama Y, Yoshimura K, Iida H (2012a) Organellar mechanosensitive 1 channels in fission yeast regulate the hypo-osmotic shock response. Nat Commun 3:1020

    Article  Google Scholar 

  • Nakayama Y, Yoshimura K, Iida H (2012b) A gain-of-function mutation in gating of Corynebacterium glutamicum NCgl1221 causes constitutive glutamate secretion. Appl Environ Microbiol 78(15):5432–5434

    Article  CAS  Google Scholar 

  • Nakayama Y, Yoshimura K, Iida H (2013) Electrophysiological characterization of the mechanosensitive channel MscCG in Corynebacterium glutamicum. Biophys J 105(6):1366–1375

    Article  CAS  Google Scholar 

  • Nakayama Y, Hirata A, Iida H (2014) Mechanosensitive channels Msy1 and Msy2 are required for maintaining organelle integrity upon hypoosmotic shock in Schizosaccharomyces pombe. FEMS Yeast Res 14(6):992–994

    Article  CAS  Google Scholar 

  • Nakayama Y, Komazawa K, Bavi N, Hashimoto K, Kawasaki H, Martinac B (2018) Evolutionary specialization of MscCG, an MscS-like mechanosensitive channel, in amino acid transport in Corynebacterium glutamicum. Sci Rep 27;8(1):12893. https://doi.org/10.1038/s41598-018-31219-6

  • Nara T, Samejima H, Kinoshita S (1964) Effect of penicillin on amino acid fermentation. Agric Biol Chem 28(2):120–124

    Article  Google Scholar 

  • Nomura T et al (2012) Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci U S A 109(22):8770–8775

    Article  CAS  Google Scholar 

  • Nottebrock D, Meyer U, Kramer R, Morbach S (2003) Molecular and biochemical characterization of mechanosensitive channels in Corynebacterium glutamicum. FEMS Microbiol Lett 218(2):305–309

    Article  CAS  Google Scholar 

  • Pivetti CD et al (2003) Two families of mechanosensitive channel proteins. Microbiol Mol Biol Rev 44 67(1):66–85

    Article  CAS  Google Scholar 

  • Pliotas C et al (2015) The role of lipids in mechanosensation. Nat Struct Mol Biol 22(12):991–998

    Article  CAS  Google Scholar 

  • Radmacher E et al (2005) Ethambutol, a cell wall inhibitor of Mycobacterium tuberculosis, elicits L glutamate efflux of Corynebacterium glutamicum. Microbiology 151(Pt 5):1359–1368

    Article  CAS  Google Scholar 

  • Ridone P, Nakayama Y, Martinac B, Battle AR (2015) Patch clamp 1 characterization of the effect of cardiolipin on MscS of E. coli. Eur Biophys J 44(7):567–576

    Article  CAS  Google Scholar 

  • Ridone P et al (2018) “Force-from-lipids” gating of mechanosensitive channels modulated by PUFAs. J Mech Behav Biomed Mater 79:158–167

    Article  CAS  Google Scholar 

  • Rosholm KR et al (2017) Activation of the mechanosensitive ion channel MscL by mechanical stimulation of supported droplet-hydrogel bilayers. Sci Rep 7:45180

    Article  CAS  Google Scholar 

  • Ruffert S, Lambert C, Peter H, Wendisch VF, Krämer R (1997) Efflux of compatible solutes in Corynebacterium glutamicum mediated by osmoregulated channel activity. Eur J Biochem 247(2):572–580

    Article  CAS  Google Scholar 

  • Sawada Y, Sokabe M (2015) Molecular dynamics study on protein-water interplay in the mechanogating of the bacterial mechanosensitive channel MscL. Eur Biophys J 44(7):531–543

    Article  CAS  Google Scholar 

  • Sawada Y, Murase M, Sokabe M (2012) The gating mechanism of the bacterial mechanosensitive channel MscL revealed by molecular dynamics simulations: from tension sensing to channel opening. Channels (Austin) 6(4):317–331

    Article  CAS  Google Scholar 

  • Shiio I, Otsuka SI, Takahashi M (1962) Effect of biotin on the bacterial formation of glutamic acid. I. Glutamate formation and cellular premeability of amino acids. J Biochem 51:56–62

    Article  CAS  Google Scholar 

  • Sotomayor M, Vasquez V, Perozo E, Schulten K (2007) Ion conduction through MscS as determined by electrophysiology and simulation. Biophys J 92(3):886–902

    Article  CAS  Google Scholar 

  • Sukharev SI, Martinac B, Arshavsky VY, Kung C (1993) Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys J 65(1):177–183

    Article  CAS  Google Scholar 

  • Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone Nature 368(6468):265–268

    Article  CAS  Google Scholar 

  • Sun Y, Sun TL, Huang HW (2014) Physical properties of Escherichia coli spheroplast membranes. Biophys J 107(9):2082–2090

    Article  CAS  Google Scholar 

  • Takinami K, Yoshii H, Tsuri H, Okada H (1965) Biochemical effects of fatty acid and its derivatives on L-glutamin acid fermentation. Agric Biol Chem 29(4):351–359

    CAS  Google Scholar 

  • Teng J, Loukin S, Anishkin A, Kung C (2015) The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflugers Arch 467(1):27–37

    Article  CAS  Google Scholar 

  • Udaka S (1960) Screening method for microorganisms accumulating metabolites and its use in the isolation of Micrococcus glutamicus. J Bacteriol 79:754–755

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y et al (2018) A novel Corynebacterium glutamicum l-glutamate exporter. Appl Environ Microbiol 84(6)

  • Wilson ME, Maksaev G, Haswell ES (2013) MscS-like mechanosensitive channels in plants and microbes. Biochemistry 52(34):5708–5722

    Article  CAS  Google Scholar 

  • Zou Y et al (2016) A gain-of-function mutation in Msl10 triggers cell death and wound-induced hyperaccumulation of jasmonic acid in Arabidopsis. J Integr Plant Biol 58(6):600–609

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the Japanese Society for Promotion of Science (JSPS) for a fellowship to YN, and the National Health and Medical Research Council of Australia for a Principal Research Fellowship to BM.

Author information

Authors and Affiliations

  1. Molecular Cardiology and Biophysics Division, Victor Chang Cardiac Research Institute, 405 Liverpool Street, Darlinghurst, NSW, 2010, Australia

    Yoshitaka Nakayama & Boris Martinac

  2. Department of Green and Sustainable Chemistry, Tokyo Denki University, 5 Asahi-cho, Senju, Adachi-ku, Tokyo, 120-8551, Japan

    Ken-ichi Hashimoto & Hisashi Kawasaki

  3. Mechanobiology Laboratory, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, 466-8550, Japan

    Yasuyuki Sawada & Masahiro Sokabe

  4. St Vincent’s Clinical School, Faculty of Medicine, University of New South Wales, Darlinghurst, NSW, 2010, Australia

    Boris Martinac

Authors
  1. Yoshitaka Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ken-ichi Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasuyuki Sawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masahiro Sokabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hisashi Kawasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Boris Martinac
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y. N., Y. S., H. K., and B. M. wrote the manuscript.

Corresponding author

Correspondence to Yoshitaka Nakayama.

Ethics declarations

Funding

This work was supported by the Discovery Project DP180102813 grant from the Australian Research Council.

Conflict of interest

Yoshitaka Nakayama declares that he has no conflicts of interest. Ken-ichi Hashimoto declares that he has no conflicts of interest. Yasuyuki Sawada declares that he has no conflicts of interest. Masahiro Sokabe declares that he has no conflicts of interest. Hisashi Kawasaki declares that he has no conflicts of interest. Boris Martinac declares that he has no conflicts of interest.

Ethical approval

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakayama, Y., Hashimoto, Ki., Sawada, Y. et al. Corynebacterium glutamicum mechanosensitive channels: towards unpuzzling “glutamate efflux” for amino acid production. Biophys Rev 10, 1359–1369 (2018). https://doi.org/10.1007/s12551-018-0452-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12551-018-0452-1

Keywords

Search

Navigation