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Classification of Acetic Acid Bacteria and Their Acid Resistant Mechanism

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Classification of Acetic Acid Bacteria and Their Acid Resistant Mechanism Qiu et al. AMB Expr (2021) 11:29 https://doi.org/10.1186/s13568-021-01189-6 MINI-REVIEW Open Access Classifcation of acetic acid bacteria and their acid resistant mechanism Xiaoman Qiu1,2, Yao Zhang1,2 and Housheng Hong1,2* Abstract Acetic acid bacteria (AAB) are obligate aerobic Gram-negative bacteria that are commonly used in vinegar fermenta- tion because of their strong capacity for ethanol oxidation and acetic acid synthesis as well as their acid resistance. However, low biomass and low production rate due to acid stress are still major challenges that must be overcome in industrial processes. Although acid resistance in AAB is important to the production of high acidity vinegar, the acid resistance mechanisms of AAB have yet to be fully elucidated. In this study, we discuss the classifcation of AAB species and their metabolic processes and review potential acid resistance factors and acid resistance mechanisms in various strains. In addition, we analyze the quorum sensing systems of Komagataeibacter and Gluconacetobacter to provide new ideas for investigation of acid resistance mechanisms in AAB in the form of signaling pathways. The results presented herein will serve as an important reference for selective breeding of high acid resistance AAB and optimization of acetic acid fermentation processes. Keywords: Acetic acid bacteria, Genus and species classifcation, Metabolic regulatory, Acid resistance mechanism, Quorum sensing, Signaling pathways Key points (Chouaia et al. 2014; Kersters et al. 2006; Sengun and Karabiyikli 2011; Soemphol et al. 2011; Trček and Barja • Summarize the current classifcation of AAB (19 gen- 2015). When compared with other bacteria, AAB show era and 92 species) in detail for the frst time; high variability (Azuma et al. 2009). Terefore, the tax- • Investigate the acid resistance mechanism in AAB onomy of AAB has undergone a long process of develop- systematically and comprehensively; ment that started with an initial phenotypic classifcation • Explain the acid resistance mechanism from the new and continued as the polyphasic classifcation approach perspective of signal pathways. became available. Polyphasic classifcation mainly includes phenotypic, chemical, and genetic classifcation methods (Greenberg et al. 2006; Lisdiyanti et al. 2006). Introduction In the past few decades, the development of molecular Acetic acid bacteria (AAB), which are also known as Ace- biology techniques has further refned the biological clas- tobacter sp., are obligate aerobic Gram-negative bacteria sifcation of AAB. However, as things stand at present, found in the Alphaproteobacteria class, Rhodospirilla- no researchers have summarized the newly discovered les order, and Acetobacteraceae family (Kersters 2006). specifc genus and species classifcation of AAB system- AAB are often found in warm and humid regions, in atically, except for a 2008 article that only summarized fruits, fowers, fruit fy guts, and some fermented foods the 10 genus and 45 species (Cleenwerck and Vos 2008), which is a major focus of our article. *Correspondence: [email protected] Major metabolic pathways in AAB include the ethanol 1 College of Biotechnology and Pharmaceutical Engineering, Nanjing oxidation respiratory chain pathway, tricarboxylic acid Tech University, No. 30, Puzhu Road, Nanjing 211800, China cycle pathway, pyruvate metabolic pathway, and pentose Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. Qiu et al. AMB Expr (2021) 11:29 Page 2 of 15 phosphate pathway. Among these, the most signifcant respiratory chain coenzyme they contained (Asai 1935; reaction is the incomplete oxidation of sugars, alcohols, Yamada et al. 1983, 2012). With the development of poly- or sugar alcohols into aldehydes, ketones, and organic phasic classifcation techniques, new genera and species acids (Sengun 2017). Te greatest strength of AAB is have been continuously found (Cleenwerck 2008), and their ability to use less biomass to produce large amounts 19 genera and 92 species of AAB have been identifed of acetic acid compared to other bacterias that produce to date (Table 1). AAB are mainly used in the industrial organic acids (López-Garzón and Straathof 2014); there- production of vinegars and fruit vinegar beverages, with fore, they are important industrial microorganisms that Acetobacter and Komagataeibacter being primarily used are widely used in the production of vinegar and fruit in vinegar making (Kanchanarach et al. 2010; Wu et al. vinegar, gluconic acid products, and development of bio- 2012). fuel cells (Lynch et al. 2019; Misra et al. 2012; Sainz et al. 2016). Acetobacter Te presence of acetic acid in vinegar products makes Acetobacter uses two membrane-bound enzymes (alco- AAB fermentation unique (Zhang et al. 2016; Zheng hol dehydrogenase (ADH) and acetaldehyde dehydro- et al. 2018). Specifcally, acetic acid changes the favor genase (ALDH)) to oxidize ethanol to acetic acid during of vinegar and increases the survival advantages of AAB respiration, after which it further oxidizes acetic acid and (Lynch et al. 2019; Hong 2016, 2017); however, acetic lactic acid to carbon dioxide and water. However, Aceto- acid accumulation causes acid stress that inhibits AAB bacter are unable to utilize sugar alcohols such as glyc- growth (Trček et al. 2015). During fermentation, the erol, sorbitol, and mannitol to produce acetic acid. Te large number of dehydrogenases on the cell membrane respiratory chain coenzyme (CoQ) used by Acetobacter of AAB causes the incomplete oxidation of many carbon is Q9 (Kersters et al. 2006). sources into acetic acid (Matsushita et al. 2016). Because At present, the main strains used in industrial produc- of the incomplete glycolysis, the main energy sources for tion of acetic acid in China are A. pasteurianus Zhongke maintaining cellular homeostasis are from the respiratory AS1.41 and Huniang 1.01 (Chen et al. 2017), which are chain, tricarboxylic acid cycle, and pentose phosphate relatively uniform. Damage will occur in Acetobacter pathway (Illeghems et al. 2013). Resistance towards highly strains when the acetic acid concentration reaches 7–8%; acidic environments requires large amounts of energy, therefore, these strains are mainly used in conventional which severely limits cell growth. As a result, AAB with surface production of vinegar and the fnal acid concen- high acid resistance can increase acetic acid productivity tration usually does not exceed 8%, with a maximum and conversion rate, thereby increasing the bioconver- acidity of 9–10% (Andrés-Barrao et al. 2016). A recent sion efciency of acetic acid. Hence, elucidation of acid study reported that A. pasteurianus could produce ace- resistance mechanisms can provide important guidance tic acid in a two-stage aeration protocol with a maximum for the selective breeding of acetic acid-producing bacte- acidity of 9.33% (Qi et al. 2014). In addition, strains iso- ria and bioconversion of high acidity vinegar. lated from traditional vinegars such as Chinese grain vin- We found that most researchers only wrote part of the egar, Japanese Komesu and Kurosu vinegars, and South acid resistance mechanism of AAB and none of them Korean black raspberry vinegar are mainly A. pasteuri- described the relationship between the quorum sensing anus (Nanda et al. 2001; Song et al. 2016; Wang 2016). and acid resistance mechanism of AAB. In this review, we discuss the specifc classifcation of AAB for the frst Komagataeibacter time and its metabolic pathways before systematically Komagataeibacter can oxidize ethanol to acetic acid and and comprehensively summarizing the latest studies on oxidize acetic acid to carbon dioxide and water (Yamada acid resistance in AAB. In addition, we analyze the quo- et al. 2012). Te respiratory chain CoQ used by Koma- rum sensing systems of Komagataeibacter and Glucon- gataeibacter is Q10 (Kersters et al. 2006). Members of acetobacter to elucidate acid resistance mechanisms in this genus are characterized by an absence of fagella AAB from a new perspective of signal pathways. and inability to produce brown compounds. In addition, some strains can produce cellulose, show an inability to Overview of AAB and its taxonomy produce 2,5-diketo-D-gluconate, are able to produce Tere are many types of AAB, among which the frst dihydroxyacetone from glycerol, and can oxidize glucose, genus, Acetobacter, was frst proposed and described by galactose, xylose, arabinoside, and ethanol to produce Beijerinck in 1898 (Beijerinck 1898). Subsequently, four organic acids. major genera (Acetobacter, Gluconobaeter, Gluconace- Komagataeibacter strains, which can resist 15–20% tobacter, and Komagataeibacter) were confrmed based acetic acid, are mainly used to produce fruit vinegar and on their ethanol oxidation capabilities and the type of alcoholic vinegar in liquid-state deep fermentation in Qiu et al. AMB Expr (2021) 11:29 Page 3 of 15 Table 1 Current classifcation of the Acetobacteraceae (19 genera, 92 species) Speciesa DNA G C(mol%)b References Speciesa DNA G C(mol%)b References + + Acetobacter aceti 56.4–58.3 Lisdiyanti et al. (2000) Gluconacetobacter diazo- 61.0–63.0 Yamada et al. (1997) trophicus Acetobacter ascendens 53.2–53.3 Kim et al. (2018) Gluconacetobacter 58.0 Lisdiyanti et al. (2006) entanii Acetobacter cerevisiae 56.0–57.6 Iino et al. (2012) Gluconacetobacter 57.96–67.5 Nishijima et al.
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