Abstract
Acetic acid bacteria (AAB) are a group of gram-negative or gram-variable bacteria which possess an obligate aerobic property with oxygen as the terminal electron acceptor, meanwhile transform ethanol and sugar to corresponding aldehydes, ketones and organic acids. Since the first genus Acetobacter of AAB was established in 1898, 16 AAB genera have been recorded so far. As the main producer of a world-wide condiment, vinegar, AAB have evolved an elegant adaptive system that enables them to survive and produce a high concentration of acetic acid. Some researches and reviews focused on mechanisms of acid resistance in enteric bacteria and made the mechanisms thoroughly understood, while a few investigations did in AAB. As the related technologies with proteome, transcriptome and genome were rapidly developed and applied to AAB research, some plausible mechanisms conferring acetic acid resistance in some AAB strains have been published. In this review, the related mechanisms of AAB against acetic acid with acetic acid assimilation, transportation systems, cell morphology and membrane compositions, adaptation response, and fermentation conditions will be described. Finally, a framework for future research for anti-acid AAB will be provided.
Similar content being viewed by others
References
Adams MR (1998) Vinegar. In: Wood BB (ed) Microbiology of fermented foods. Springer, pp 1–44
Alauzet C, Teyssier C, Jumas-Bilak E, Gouby A, Chiron R, Rabaud C, Counil F, Lozniewski A, Marchandin H (2010) Gluconobacter as well as Asaia species, newly emerging opportunistic human pathogens among acetic acid bacteria. J Clin Microbiol 48(11):3935–3942
Andrés-Barrao C, Saad MM, Chappuis M-L, Boffa M, Perret X, Ortega Pérez R, Barja F (2012) Proteome analysis of Acetobacter pasteurianus during acetic acid fermentation. J Proteomics 75(6):1701–1717
Axe DD, Bailey JE (1995) Transport of lactate and acetate through the energized cytoplasmic membrane of Escherichia coli. Biotechnol Bioeng 47(1):8–19
Azcarate-Peril MA, Altermann E, Hoover-Fitzula RL, Cano RJ, Klaenhammer TR (2004) Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Appl Environ Microb 70(9):5315–5322
Azuma Y, Hosoyama A, Matsutani M, Furuya N, Horikawa H, Harada T, Hirakawa H, Kuhara S, Matsushita K, Fujita N (2009) Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus. Nucleic Acids Res 37(17):5768–5783
Bartowsky EJ, Henschke PA (2008) Acetic acid bacteria spoilage of bottled red wine-a review. Int J Food Microbiol 125:60–70
Bastián F, Cohen A, Piccoli P, Luna V, Bottini R, Baraldi R (1998) Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regul 24(1):7–11
Bearson S, Bearson B, Foster JW (1997) Acid stress responses in enterobacteria. FEMS Microbiol Lett 147(2):173–180
Beijerinck M (1898) Ueber die arten der essigbakterien. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 4:209–216
Chang YY, Cronan JE (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33(2):249–259
Chen F, Li L, Qu J, Chen C (2009) Cereal vinegars made by solid-state fermentation in China. In: Solieri L, Giudici P (eds) Vinegars of the world. Springer, Milan, pp 243–259
Chinnawirotpisan P, Theeragool G, Limtong S, Toyama H, Adachi OO, Matsushita K (2003) Quinoprotein alcohol dehydrogenase is involved in catabolic acetate production, while NAD-dependent alcohol dehydrogenase in ethanol assimilation in Acetobacter pasteurianus SKU1108. J Biosci Bioeng 96(6):564–571
Cleenwerck I, De Vos P (2008) Polyphasic taxonomy of acetic acid bacteria: an overview of the currently applied methodology. Int J Food Microbiol 125(1):2–14
Conner DE, Kotrola JS (1995) Growth and survival of Escherichia coli O157: H7 under acidic conditions. Appl Environ Microbiol 61(1):382–385
Cotter PD, Gahan CG, Hill C (2001) A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol Microbiol 40(2):465–475
Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol R 61(1):47–64
Diez-Gonzalez F, Russell JB (1997) The ability of Escherichia coli O157: H7 to decrease its intracellular pH and resist the toxicity of acetic acid. Microbiology 143(4):1175–1180
Drysdale GS, Fleet GH (1988) Acetic acid bacteria in winemaking: a review. Am J Enol Viticult 39(2):143–154
Entani E, Ohmori S, Masai H, Suzuki K (1985) Acetobacter polyoxogenes sp. nov., a new species of an acetic acid bacterium useful for producing vinegar with high acidity. J Gen Appl Microbiol 31:475–490
Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2(1):898–907
Fuentes-Ramírez LE, Bustillos-Cristales R, Tapia-Hernández A, Jiménez-Salgado T, Wang ET, Martínez-Romero E, Caballero-Mellado J (2001) Novel nitrogen-fixing acetic acid bacteria, Gluconacetobacter johannae sp. nov. and Gluconacetobacter azotocaptans sp. nov., associated with coffee plants. Int J Syst Evol Micr 51(4):1305–1314
Fukaya M, Takemura H, Okumura H, Kawamura Y, Horinouchi S, Beppu T (1990) Cloning of genes responsible for acetic acid resistance in Acetobacter aceti. J Bacteriol 172(4):2096–2104
Fukaya M, Takemura H, Tayama K, Okumura H, Kawamura Y, Horinouchi S, Beppu T (1993) The aarC gene responsible for acetic acid assimilation confers acetic acid resistance on Acetobacter aceti. J Ferment Bioeng 76(4):270–275
García-García I, Santos-Dueñas IM, Jiménez-Ot C, Jiménez-Hornero JE, Bonilla-Venceslada JL (2009) Vinegar engineering. In: Solieri L, Giudici P (eds) Vinegars of the world. Springer, Milan, pp 97–120
Gething M-J, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45
González A, Guillamón JM, Mas A, Poblet M (2006) Application of molecular methods for routine identification of acetic acid bacteria. Int J Food Microbiol 108(1):141–146
Gosselé F, Swings J (1986) Identification of Acetobacter liquefaciens as causal agent of pink-disease of pineapple fruit. J Phytopathol 116:167–175
Grierson B (2009) Malt and distilled malt vinegar. In: Solieri L, Giudici P (eds) Vinegars of the world. Springer, Milan, pp 135–143
Gu CQ, Chen WL, Zheng ZM, Zhu DX, Lai JP, Lin JY, Lai YP, Zeng QZ, Zhou YQ (2010) Vinegar production from pineapple waste by semi-solid state fermentation. Food Sci 31(16):56–60
Gullo M, Giudici P (2008) Acetic acid bacteria in traditional balsamic vinegar: phenotypic traits relevant for starter cultures selection. Int J Food Microbiol 125(1):46–53
Gullo M, Mamlouk D, De Vero L, Giudici P (2012) Acetobacter pasteurianus strain AB0220: cultivability and phenotypic stability over 9 years of preservation. Curr Microbiol 64(6):576–580
Gullo M, Verzelloni E, Canonico M (2014) Aerobic submerged fermentation by acetic acid bacteria for vinegar production: process and biotechnological aspects. Process Biochem 49:1571–1579
Hattori H, Yakushi T, Matsutani M, Moonmangmee D, Toyama H, Adachi O, Matsushita K (2012) High-temperature sorbose fermentation with thermotolerant Gluconobacter frateurii CHM43 and its mutant strain adapted to higher temperature. Appl Microbiol Biot 95(6):1531–1540
Hecker M, Schumann W, Völker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19(3):417–428
Ishikawa M, Okamoto-Kainuma A, Jochi T, Suzuki I, Matsui K, Kaga T, Koizumi Y (2010a) Cloning and characterization of grpE in Acetobacter pasteurianus NBRC 3283. J Biosci Bioeng 109(1):25–31
Ishikawa M, Okamoto-Kainuma A, Matsui K, Takigishi A, Kaga T, Koizumi Y (2010b) Cloning and characterization of clpB in Acetobacter pasteurianus NBRC 3283. J Biosci Bioeng 110(1):69–71
Iyer PR, Geib SM, Catchmark J, Kao T-H, Tien M (2010) Genome sequence of a cellulose-producing bacterium, Gluconacetobacter hansenii ATCC 23769. J Bacteriol 192(16):4256
Ji A, Gao P (2001) Substrate selectivity of Gluconobacter oxydans for production of 2, 5-diketo-d-gluconic acid and synthesis of 2-keto-l-gulonic acid in a multienzyme system. Appl Biochem Biotech 94(3):213–223
Kanchanarach W, Theeragool G, Inoue T, Yakushi T, Adachi O, Matsushita K (2010) Acetic acid fermentation of Acetobacter pasteurianus: relationship between acetic acid resistance and pellicle polysaccharide formation. Biosci Biotech Bioch 74(8):1591–1597
Karpowich N, Martsinkevich O, Millen L, Yuan Y-R, Dai PL, MacVey K, Thomas PJ, Hunt JF (2001) Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure 9(7):571–586
Kashima Y, Iijima M, Nakano T, Tayama K, Koizumi Y, Udaka S, Yanagida F (2000) Role of intracellular esterases in the production of esters by Acetobacter pasteurianus. J Biosci Bioeng 89(1):81–83
Kregiel D, Rygala A, Libudzisz Z, Walczak P, Oltuszak-Walczak E (2012) Asaia lannensis—the spoilage acetic acid bacteria isolated from strawberry-flavored bottled water in Poland. Food Control 26:147–150
Lin J, Smith MP, Chapin KC, Baik HS, Bennett GN, Foster JW (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microb 62:3094–3100
Mah T-FC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39
Malimas T, Yukphan P, Takahashi M, Muramatsu Y, Kaneyasu M, Potacharoen W, Tanasupawat S, Nakagawa Y, Tanticharoen M, Yamada Y (2009) Gluconobacter japonicus sp. nov., an acetic acid bacterium in the alphaproteobacteria. Int J Syst Evol Micr 59(3):466–471
Mamlouk D, Gullo M (2013) Acetic acid bacteria: physiology and carbon sources oxidation. Indian J Microbiol 53(4):377–384
Matsushita K, Toyama H, Adachi O (2004) Respiratory chains in acetic acid bacteria: membrane bound periplasmic sugar and alcohol respirations respiration in archaea and bacteria. Springer, Netherlands, pp 81–99
Matsushita K, Inoue T, Adachi O, Toyama H (2005) Acetobacter aceti possesses a proton motive force-dependent efflux system for acetic acid. J Bacteriol 187(13):4346–4352
Merfort M, Herrmann U, Ha SW, Elfari M, Bringer-Meyer S, Görisch H, Sahm H (2006) Modification of the membrane-bound glucose oxidation system in Gluconobacter oxydans significantly increases gluconate and 5-keto-d-gluconic acid accumulation. Biotechnol J 1(5):556–563
Mesa MM, Caro I, Cantero D (1996) Viability reduction of Acetobacter aceti due to the absence of oxygen in submerged cultures. Biotechnol Progr 12(5):709–712
Moore JE, McCalmont M, Xu J, Millar BC, Heaney N (2002) Asaia sp., an unusual spoilage organism of fruit-flavored bottled water. Appl Environ Microb 68:4130–4131
Mullins EA, Francois JA, Kappock TJ (2008) A specialized citric acid cycle requiring succinyl-coenzyme A (CoA): acetate CoA-transferase (AarC) confers acetic acid resistance on the acidophile Acetobacter aceti. J Bacteriol 190(14):4933–4940
Murooka Y, Nanda K, Yamashita M (2009) Rice vinegars. In: Solieri L, Giudici P (eds) Vinegars of the world. Springer, Milan, pp 121–133
Nakano S, Fukaya M (2008) Analysis of proteins responsive to acetic acid in Acetobacter: molecular mechanisms conferring acetic acid resistance in acetic acid bacteria. Int J Food Microbiol 125(1):54–59
Nakano S, Fukaya M, Horinouchi S (2004) Enhanced expression of aconitase raises acetic acid resistance in Acetobacter aceti. FEMS Microbiol Lett 235(2):315–322
Nakano S, Fukaya M, Horinouchi S (2006) Putative ABC transporter responsible for acetic acid resistance in Acetobacter aceti. Appl Environ Microb 72(1):497–505
Nanda K, Taniguchi M, Ujike S, Ishihara N, Mori H, Ono H, Murooka Y (2001) Characterization of acetic acid bacteria in traditional acetic acid fermentation of rice vinegar (komesu) and unpolished rice vinegar (kurosu) produced in Japan. Appl Environ Microb 67(2):986–990
Nguyen VT, Flanagan B, Gidley MJ, Dykes GA (2008) Characterization of cellulose production by a Gluconacetobacter xylinus strain from Kombucha. Curr Microbiol 57(5):449–453
Nomura M, Nakajima I, Fujita Y, Kobayashi M, Kimoto H, Suzuki I, Aso H (1999) Lactococcus lactis contains only one glutamate decarboxylase gene. Microbiology 145(6):1375–1380
Ogino H, Azuma Y, Hosoyama A, Nakazawa H, Matsutani M, Hasegawa A, Otsuyama K-I, Matsushita K, Fujita N, Shirai M (2011) Complete genome sequence of NBRC 3288, a unique cellulose-nonproducing strain of Gluconacetobacter xylinus isolated from vinegar. J Bacteriol 193(24):6997–6998
Okamoto-Kainuma A, Yan W, Kadono S, Tayama K, Koizumi Y, Yanagida F (2002) Cloning and characterization of groESL operon in Acetobacter aceti. J Biosci Bioeng 94(2):140–147
Okamoto-Kainuma A, Yan W, Fukaya M, Tukamoto Y, Ishikawa M, Koizumi Y (2004) Cloning and characterization of the dnaKJ operon in Acetobacter aceti. J Biosci Bioeng 97(5):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(4):429–432
Okumura TUTBH (1985) Biochemical characteristics of spontaneous mutants of Acetobacter aceti deficient in ethanol oxidation. Agric Biol Chem 49(8):2485–2487
Piper P, Mahe Y, Thompson S, Pandjaitan R, Holyoak C, Egner R, Mühlbauer M, Coote P, Kuchler K (1998) The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J 17(15):4257–4265
Prieto C, Jara C, Mas A, Romero J (2007) Application of molecular methods for analysing the distribution and diversity of acetic acid bacteria in Chilean vineyards. Int J Food Microbiol 115(3):348–355
Qi ZL, Wang W, Yang HL, Xia XL, Yu XB (2014) Mutation of Acetobacter pasteurianus by UV irradiation under acidic stress for high-acidity vinegar fermentation. Int J Food Sci Tech 49:468–476
Raspor P, Goranovic D (2008) Biotechnological applications of acetic acid bacteria. Crit Rev Biotechnol 28(2):101–124
Rollan G, Lorca G, Font de Valdez G (2003) Arginine catabolism and acid tolerance response in Lactobacillus reuteri isolated from sourdough. Food Microbiol 20(3):313–319
Russell J (1992) Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling. J Appl Microbiol 73(5):363–370
Sakurai K, Arai H, Ishii M, Igarashi Y (2011) Transcriptome response to different carbon sources in Acetobacter aceti. Microbiology 157(3):899–910
Schüller G, Hertel C, Hammes WP (2000) Gluconacetobacter entanii sp. nov., isolated from submerged high-acid industrial vinegar fermentations. Int J Syst Evol Microbiol 50:2013–2020
Shinagawa E, Toyama H, Matsushita K, Tuitemwong P, Theeragool G, Adachi O (2008) Formaldehyde elimination with formaldehyde and formate oxidase in membrane of acetic acid bacteria. J Biosci Bioeng 105(3):292–295
Sokollek SJ, Hertel C, Hammes WP (1998a) Description of Acetobacter oboediens sp. nov. and Acetobacter pomorum sp. nov., two new species isolated from industrial vinegar fermentations. Int J Syst Bacteriol 48(3):935–940
Sokollek SJ, Hertel C, Hammes WP (1998b) Cultivation and preservation of vinegar bacteria. J Biotechnol 60:195–206
Solieri L, Giudici P (2008) Yeasts associated to traditional balsamic vinegar: ecological and technological features. Int J Food Microbiol 125(1):36–45
Solieri L, Giudici P (2009) Vinegars of the world. Springer, Milan, pp 1–16
Švitel J, Šturdik E (1995) 2-Ketogluconic acid production by Acetobacter pasteurianus. Appl Biochem Biotech 53(1):53–63
Takemura H, Kondo K, Horinouchi S, Beppu T (1993) Induction by ethanol of alcohol dehydrogenase activity in Acetobacter pasteurianus. J Bacteriol 175(21):6857–6866
Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69(4):2313–2320
Thi Lan Vu H, Yukphan P, Chaipitakchonlatarn W, Malimas T, Muramatsu Y, Thi Tu Bui U, Tanasupawat S, Cong Duong K, Nakagawa Y, Thanh Pham H, Yamada Y (2013) Nguyenibacter vanlangensis gen. nov., sp. nov., an unusual acetic acid bacterium in the α-proteobacteria. J Gen Appl Microbiol 59(2):153–166
Torija M, Mateo E, Guillamón J, Mas A (2010) Identification and quantification of acetic acid bacteria in wine and vinegar by TaqMan–MGB probes. Food Microbiol 27(2):257–265
Trcek J, Toyama H, Czuba J, Misiewicz A, Matsushita K (2006) Correlation between acetic acid resistance and characteristics of PQQ-dependent ADH in acetic acid bacteria. Appl Microbiol Biot 70(3):366–373
Trček J, Jernejc K, Matsushita K (2007) The highly tolerant acetic acid bacterium Gluconacetobacter europaeus adapts to the presence of acetic acid by changes in lipid composition, morphological properties and PQQ-dependent ADH expression. Extremophiles 11(4):627–635
Trowsdale J, Hanson I, Mockridge I, Beck S, Townsendt A, Kelly A (1990) Sequences encoded in the class II region of the MHC related to the ABC superfamily of transporters. Nature 348:741–744
Vegas C, Mateo E, González Á, Jara C, Guillamón JM, Poblet M, Torija MJ, Mas A (2010) Population dynamics of acetic acid bacteria during traditional wine vinegar production. Int J Food Microbiol 138(1):130–136
Wu JJ, Gullo M, Chen FS, Giudici P (2010) Diversity of Acetobacter pasteurianus strains isolated from solid-state fermentation of cereal vinegars. Curr Microbiol 60(4):280–286
Wu JJ, Ma YK, Zhang FF, Chen FS (2012) Biodiversity of yeasts, lactic acid and acetic acid bacteria in the fementation of “Shanxi aged vinegar”, a traditional Chinese vinegar. Food Microbiol 30(1):289–297
Yamada Y, Yukphan P, Lan Vu HT, Muramatsu Y, Ochaikul D, Tanasupawat S, Nakagawa Y (2012) Description of Komagataeibacter gen. nov., with proposals of new combinations (Acetobacteraceae). J Gen Appl Microbiol 58(5):397–404
Yukphan P, Malimas T, Muramatsu Y, Takahashi M, Kaneyasu M, Tanasupawat S, Nakagawa Y, Suzuki K-I, Potacharoen W, Yamada Y (2008) Tanticharoenia sakaeratensis gen. nov., sp. nov., a new osmotolerant acetic acid bacterium in the α-proteobacteria. Biosci Biotech Bioch 72(3):672–676
Yukphan P, Malimas T, Muramatsu Y, Takahashi M, Kaneyasu M, Potacharoen W, Tanasupawat S, Nakagawa Y, Hamana K, Tahara Y (2009) Ameyamaea chiangmaiensis gen. nov., sp. nov., an acetic acid bacterium in the α-proteobacteria. Biosci Biotech Bioch 73(10):2156–2162
Yukphan P, Malimas T, Muramatsu Y, Potacharoen W, Tanasupawat S, Nakagawa Y, Tanticharoen M, Yamada Y (2011) Neokomagataea gen. nov., with descriptions of Neokomagataea thailandica sp. nov. and Neokomagataea tanensis sp. nov., osmotolerant acetic acid bacteria of the α-proteobacteria. Biosci Biotech Bioch 75(3):419–426
Acknowledgments
This study was supported by Programs of International S & T Cooperation, Ministry of Science and Technology, P. R. China (No. 2014DFG32380), and the Fundamental Research Funds for the Central Universities (No. 2013PY006).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, B., Shao, Y. & Chen, F. Overview on mechanisms of acetic acid resistance in acetic acid bacteria. World J Microbiol Biotechnol 31, 255–263 (2015). https://doi.org/10.1007/s11274-015-1799-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-015-1799-0