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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
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
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
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 Å. Nature (London) 371:578–586
DeSantis ME, Shorter J (2012) The elusive middle domain of Hsp104 and clpB: location and function. Biochim Biophys Acta 1823:29–39
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
Ewalt KL, Hendrick JP, Houry WA, Hartl FU (1997) In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90:491–500
Fan CY, Lee S, Cyr DM (2003) Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 8:309–316
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
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
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
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
Harrison C (2003) GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8:218–224
Hartle FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858
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
Horwich AL, Farr GW, Fenton WA (2006) GroEL–GroES-mediated protein folding. Chem Rev 106:1917–1930
Hunt JF, Weavr AJ, Landry SJ, Gierasch L, Deisenhofer J (1996) The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature (London) 379:37–45
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
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
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
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
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
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
Mande SC, Mehra V, Bloom BR, Hol WGJ (1996) Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae. Science 271:203–207
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
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
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
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
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
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
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
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
Paget MSB, Helmann JD (2003) The σ70 family of sigma factors. Genome Biol 4:203
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
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
Schirmer EC, Glover JR, Singer MA, Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21:289–296
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
Segal G, Ron EZ (1996a) Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol Lett 138:1–10
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
Segal G, Ron EZ (1998) Regulation of heat-shock response in bacteria. Ann N Y Acad Sci 851:147–151
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
Steiner P, Sauer U (2001) Proteins induced during adaptation of Acetobacter aceti to high acetate concentrations. Appl Environ Microbiol 67:5474–5481
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
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
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
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
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
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
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
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
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-4-431-55933-7_8
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55931-3
Online ISBN: 978-4-431-55933-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)