Skip to main content

Physiology of Acetobacter spp.: Involvement of Molecular Chaperones During Acetic Acid Fermentation

  • Chapter
  • First Online:
Acetic Acid Bacteria

Abstract

Acetic acid bacteria produce acetic acid from ethanol to acquire energy through a process called acetic acid fermentation. These bacteria are inevitably exposed to various stressors during fermentation but have developed resistance to these stressors. These resistance properties have been attributed to the combination of several kinds of mechanisms, including the role of molecular chaperones. In this chapter, we outline the involvement of major molecular chaperones (GroESL, DnaKJ, GrpE, and ClpB) in the stress-resistant abilities of Acetobacter pasteurianus NBRC3283, in addition to the role of the regulatory factor RpoH, with reference to our recent studies using proteomic analyses, RNA-seq analyses, and the mutants of these chaperones.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Andrés-Barrao C, Saad MM, Chappuis ML, Boffa M, Perret X, Pérez RO, Barja F (2012) Proteome analysis of Acetobacter pasteurianus during acetic acid fermentation. J Proteomics 75:1701–1717

    Article  PubMed  Google Scholar 

  • Azuma Y, Hosoyama A, Matsutani M, Furuya N, Horikawa H, Harada T, Hirakawa H, Kuhara S, Matsushita K, Fujita N, Shirai M (2009) Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus. Nucleic Acids Res 37:5768–5783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bralg K, Othwlnowsk Z, Hegde R, Bolsvert DC, Joachimiak A, Horwich AL, Sigler PB (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 Ã…. Nature (London) 371:578–586

    Article  Google Scholar 

  • DeSantis ME, Shorter J (2012) The elusive middle domain of Hsp104 and clpB: location and function. Biochim Biophys Acta 1823:29–39

    Article  CAS  PubMed  Google Scholar 

  • Erickson JW, Vaughn V, Salter WA, Neidhardt FC, Gross CA (1987) Regulation of the promoter and transcripts of rpoH, the Escherichia coli heat shock regulatory gene. Genes Dev 1:419–432

    Article  CAS  PubMed  Google Scholar 

  • Ewalt KL, Hendrick JP, Houry WA, Hartl FU (1997) In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90:491–500

    Article  CAS  PubMed  Google Scholar 

  • Fan CY, Lee S, Cyr DM (2003) Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 8:309–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genevaux P, Schwager F, Georgopouls D, Kelley WL (2001) The djlA gene acts synergistically with dnaJ in promoting Escherichia coli growth. J Bacteriol 183:5747–5750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genevaux P, Georgopoulos C, Kelley WL (2007) The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol Microbiol 66:840–857

    Article  CAS  PubMed  Google Scholar 

  • Goloubinoff P, Mogk A, Zvi APB, Tomoyasu T, Bukau B (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 96:13732–13737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guisbert E, Herman C, Lu CZ, Gross CA (2004) A chaperone network controls the heat shock response in E. coli. Genes Dev 18:2812–2821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison C (2003) GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8:218–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartle FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858

    Article  Google Scholar 

  • Hennessy F, Nicoll WS, Zimmermann R, Cheetham ME, Blatch GL (2005) Not all J domains are created equal: implications for the specificity of Hsp40–Hsp70 interactions. Protein Sci 14:1697–1709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horwich AL, Farr GW, Fenton WA (2006) GroEL–GroES-mediated protein folding. Chem Rev 106:1917–1930

    Article  CAS  PubMed  Google Scholar 

  • Hunt JF, Weavr AJ, Landry SJ, Gierasch L, Deisenhofer J (1996) The crystal structure of the GroES co-chaperonin at 2.8 Ã… resolution. Nature (London) 379:37–45

    Article  CAS  Google Scholar 

  • Ishikawa M, Okamoto-Kainuma A, Jochi T, Suzuki I, Matsui K, Kaga T, Koizumi Y (2010a) Cloning and characterization of grpE in Acetobacter pasteurianus NBRC3283. J Biosci Bioeng 109:25–31

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa M, Okamoto-Kainuma A, Matsui K, Takigishi A, Kaga T, Koizumi Y (2010b) Cloning and characterization of clpB in Acetobacter pasteurianus NBRC3283. J Biosci Bioeng 110:69–71

    Article  CAS  PubMed  Google Scholar 

  • Kannan TR, Musatovova O, Gowda P, Baseman JB (2008) Characterization of a unique ClpB protein of Mycoplasma pneumoniae and its impact on growth. Infect Immun 76:5082–5092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitagawa M, Wada C, Yoshioka S, Yura T (1991) Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32). J Bacteriol 173:4247–4253

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Sowa ME, Watanabe Y, Sigler PB, Chiu W, Yoshida M, Tsai FTF (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115:229–240

    Article  CAS  PubMed  Google Scholar 

  • Lim B, Miyazaki R, Neher S, Siegele DA, Ito K, Walter P, Akiyama Y, Yura T, Gross CA (2013) Heat shock transcription factor σ32 co-opts the signal recognition particle to regulate protein homeostasis in E. coli. PLoS Biol 11:e1001735

    Article  PubMed  PubMed Central  Google Scholar 

  • Mande SC, Mehra V, Bloom BR, Hol WGJ (1996) Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae. Science 271:203–207

    Article  CAS  PubMed  Google Scholar 

  • Matsushita K, Takai Y, Shinagawa E, Ameyama M, Adachi O (1992) Ethanol oxidase respiratory chain of acetic acid bacteria. Reactivity with ubiquinone of pyrroloquinoline quinone-dependent alcohol dehydrogenases purified from Acetobacter aceti and Gluconobacter oxydans. Biosci Biotechnol Biochem 56:304–310

    Article  CAS  Google Scholar 

  • Morita M, Kanemori M, Yanagi H, Yura T (1999) Heat-induced synthesis of σ32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J Bacteriol 181:401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakahigashi K, Yanagi H, Yura T (1995) Isolation and sequence analysis of rpoH genes encoding σ32 homologs from gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucleic Acids Res 23:4383–4390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43

    CAS  PubMed  Google Scholar 

  • Okamoto-Kainuma A, Wang Y, Kadono S, Tayama K, Kozumi Y, Yanagida F (2002) Cloning and characterization of groESL operon in Acetobacter aceti. J Biosci Bioeng 94:140–147

    Article  CAS  PubMed  Google Scholar 

  • Okamoto-Kainuma A, Wang Y, Fukaya M, Tukamoto Y, Ishikawa M, Koizumi Y (2004) Cloning and characterization of the dnaKJ operon in Acetobacter aceti. J Biosci Bioeng 97:339–342

    Article  CAS  PubMed  Google Scholar 

  • Okamoto-Kainuma A, Ishikawa M, Nakamura H, Fukazawa S, Tanaka N, Yamagami K, Koizumi Y (2011) Characterization of rpoH in Acetobacter pasteurianus NBRC3283. J Biosci Bioeng 111:429–432

    Article  CAS  PubMed  Google Scholar 

  • Okamoto-Kainuma A, Ishikawa M, Ito K, Koizumi Y (2012) Proteomic study of Acetobacter pasteurianus NBRC3283 and analysis of factors possibly related to acetic acid fermentation. Abstract book of third international conference on acetic acid bacteria, vinegar and other products, Cordoba Spain, Apr 17–20, pp 17–18

    Google Scholar 

  • Paget MSB, Helmann JD (2003) The σ70 family of sigma factors. Genome Biol 4:203

    Article  PubMed  PubMed Central  Google Scholar 

  • Perales-Calvo J, Muga A, Moro F (2010) Role of DnaJ G/F-rich domain in conformational recognition and binding of protein substrates. J Biol Chem 285:34231–34239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenzweig R, Moradi S, Zarrine-Afsar A, Glover JR, Kay LK (2013) Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science 339:1080–1083

    Article  CAS  PubMed  Google Scholar 

  • Schirmer EC, Glover JR, Singer MA, Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21:289–296

    Article  CAS  PubMed  Google Scholar 

  • Segal G, Ron EZ (1995) The dnaKJ operon of Agrobacterium tumefaciens: transcriptional analysis and evidence for a new heat shock promoter. J Bacteriol 177:5952–5958

    CAS  PubMed  PubMed Central  Google Scholar 

  • Segal G, Ron EZ (1996a) Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol Lett 138:1–10

    Article  CAS  PubMed  Google Scholar 

  • Segal G, Ron EZ (1996b) Heat shock activation of the groESL operon of Agrobacterium tumefaciens and the regulatory roles of the inverted repeat. J Bacteriol 178:3634–3640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Segal G, Ron EZ (1998) Regulation of heat-shock response in bacteria. Ann N Y Acad Sci 851:147–151

    Article  CAS  PubMed  Google Scholar 

  • Seyffer FS, Kummer E, Oguchi Y, Winker J, Kumar M, Zahn R, Sourjik V, Bukau B, Mogk A (2012) Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA; disaggregase at aggregate surfaces. Nat Struct Mol Biol 19:1347–1355

    Article  CAS  PubMed  Google Scholar 

  • Steiner P, Sauer U (2001) Proteins induced during adaptation of Acetobacter aceti to high acetate concentrations. Appl Environ Microbiol 67:5474–5481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Straus D, Walter W, Gross CA (1990) DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock synthesis and stability of σ32. Genes Dev 4:2202–2209

    Article  CAS  PubMed  Google Scholar 

  • Szabo A, Korszun R, Hartl FU, Flanagan J (1996) A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J 15:408–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tatsuta T, Tomoyasu T, Bukau B, Kitagawa M, Mori H, Karata K, Ogura T (1998) Heat shock regulation in the ftsH null mutant of Escherichia coli: dissection of stability and activity control mechanisms of σ32 in vivo. Mol Microbiol 30:583–593

    Article  CAS  PubMed  Google Scholar 

  • Teter SA, Houry WA, Ang D, Tradier T, Rockabrand D, Fischer G, Blum P, Georgopoulos C, Hartl FU (1999) Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97:755–765

    Article  CAS  PubMed  Google Scholar 

  • Tilly K, Erickson J, Sharma S, Georgopoulos C (1986) Heat shock regulatory gene rpoH mRNA level increases after heat shock in Escherichia coli. J Bacteriol 168:1155–1158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Kaguni JM (1989) A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli. J Bacteriol 171:4248–4253

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606–1614

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by MEXT (Ministry of Education, Culture, Sports, Science and Technology, Japan)-Supported Program for the Strategic Research Foundation at Private Universities, 2008–2012 (S0801025) and also MEXT-Supported Program for the Strategic Research Foundation at Private Universities, 2013–2017 (S1311017).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akiko Okamoto-Kainuma .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Japan

About this chapter

Cite this chapter

Okamoto-Kainuma, A., Ishikawa, M. (2016). Physiology of Acetobacter spp.: Involvement of Molecular Chaperones During Acetic Acid Fermentation. In: Matsushita, K., Toyama, H., Tonouchi, N., Okamoto-Kainuma, A. (eds) Acetic Acid Bacteria. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55933-7_8

Download citation

Publish with us

Policies and ethics