Acetic Acid Bacteria in the Food Industry: Systematics, Characteristics and Applications.

The group of Gram-negative bacteria capable of oxidising ethanol to acetic acid is called acetic acid bacteria (AAB). They are widespread in nature and play an important role in the production of food and beverages, such as vinegar and kombucha. The ability to oxidise ethanol to acetic acid also allows the unwanted growth of AAB in other fermented beverages, such as wine, cider, beer and functional and soft beverages, causing an undesirable sour taste. These bacteria are also used in the production of other metabolic products, for example, gluconic acid, l-sorbose and bacterial cellulose, with potential applications in the food and biomedical industries. The classification of AAB into distinct genera has undergone several modifications over the last years, based on morphological, physiological and genetic characteristics. Therefore, this review focuses on the history of taxonomy, biochemical aspects and methods of isolation, identification and quantification of AAB, mainly related to those with important biotechnological applications.

[1]  T. Uozumi,et al.  Biochemical Characteristics of Spontaneous Mutants of Acetobacter aceti Deficient in Ethanol Oxidation , 1985 .

[2]  A. Hosoyama,et al.  Complete Genome Sequence of NBRC 3288, a Unique Cellulose-Nonproducing Strain of Gluconacetobacter xylinus Isolated from Vinegar , 2011, Journal of bacteriology.

[3]  in chief George M. Garrity Bergey’s Manual® of Systematic Bacteriology , 1989, Springer New York.

[4]  J. Guillamón,et al.  Enumeration and detection of acetic acid bacteria by real-time PCR and nested PCR. , 2006, FEMS microbiology letters.

[5]  W. S. Williams,et al.  Alternative Environmental Roles for Cellulose Produced by Acetobacter xylinum , 1989, Applied and environmental microbiology.

[6]  M. Fukaya,et al.  Analysis of proteins responsive to acetic acid in Acetobacter: molecular mechanisms conferring acetic acid resistance in acetic acid bacteria. , 2008, International journal of food microbiology.

[7]  W. Soetaert,et al.  The Genus Gluconobacter Oxydans: Comprehensive Overview of Biochemistry and Biotechnological Applications , 2007, Critical reviews in biotechnology.

[8]  K. Paknikar,et al.  Applications of bacterial cellulose and its composites in biomedicine , 2015, Applied Microbiology and Biotechnology.

[9]  Yuki Muramatsu,et al.  Description of Komagataeibacter gen. nov., with proposals of new combinations (Acetobacteraceae). , 2012, The Journal of general and applied microbiology.

[10]  R. P. Ross,et al.  Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. , 2014, Food microbiology.

[11]  Fusheng Chen,et al.  Diversity of Acetobacter pasteurianus Strains Isolated From Solid-State Fermentation of Cereal Vinegars , 2010, Current Microbiology.

[12]  X. Perret,et al.  Metaproteomics and ultrastructure characterization of Komagataeibacter spp. involved in high-acid spirit vinegar production. , 2016, Food microbiology.

[13]  Genome Sequences of the High-Acetic Acid-Resistant Bacteria Gluconacetobacter europaeus LMG 18890T and G. europaeus LMG 18494 (Reference Strains), G. europaeus 5P3, and Gluconacetobacter oboediens 174Bp2 (Isolated from Vinegar) , 2011, Journal of bacteriology.

[14]  W. Ludwig,et al.  Phylogenetic identification of two major nitrogen-fixing bacteria associated with sugarcane. , 1998, Systematic and applied microbiology.

[15]  K. Kondo,et al.  GLUCONOACETOBACTER, A NEW SUBGENUS COMPRISING THE ACETATE-OXIDIZING ACETIC ACID BACTERIA WITH UBIQUINONE-10 IN THE GENUS ACETOBACTER , 1984 .

[16]  Shin-Ping Lin,et al.  Isolation and identification of cellulose-producing strain Komagataeibacter intermedius from fermented fruit juice. , 2016, Carbohydrate polymers.

[17]  Yuzo Yamada,et al.  Enzymatic Studies on the Oxidation of Sugar and Sugar Alcohol , 1969 .

[18]  P. Thonart,et al.  Simultaneous production of acetic and gluconic acids by a thermotolerant Acetobacter strain during acetous fermentation in a bioreactor. , 2016, Journal of bioscience and bioengineering.

[19]  K. Matsushita,et al.  High-temperature sorbose fermentation with thermotolerant Gluconobacter frateurii CHM43 and its mutant strain adapted to higher temperature , 2012, Applied Microbiology and Biotechnology.

[20]  K. Matsushita,et al.  Acetic acid bacteria: A group of bacteria with versatile biotechnological applications. , 2015, Biotechnology advances.

[21]  Ş. Karabıyıklı,et al.  Acetic Acid Bacteria: Fundamentals and Food Applications. , 2017 .

[22]  S. Ribeiro,et al.  Draft Genome Sequence of Komagataeibacter rhaeticus Strain AF1, a High Producer of Cellulose, Isolated from Kombucha Tea , 2014, Genome Announcements.

[23]  H. Santos,et al.  Advances in biomedical and pharmaceutical applications of functional bacterial cellulose-based nanocomposites. , 2016, Carbohydrate polymers.

[24]  Jiewen Zhao,et al.  Monitoring vinegar acetic fermentation using a colorimetric sensor array , 2013 .

[25]  M. Macías,et al.  Use of the Direct Epifluorescent Filter Technique for the Enumeration of Viable and Total Acetic Acid Bacteria from Vinegar Fermentation , 2003, Journal of Fluorescence.

[26]  E. Mateo,et al.  Acetic acid bacteria from biofilm of strawberry vinegar visualized by microscopy and detected by complementing culture-dependent and culture-independent techniques. , 2015, Food microbiology.

[27]  Ilse Cleenwerck,et al.  Polyphasic taxonomy of acetic acid bacteria: an overview of the currently applied methodology. , 2008, International journal of food microbiology.

[28]  K. Komagata,et al.  The Family Acetobacteraceae , 2014 .

[29]  Jin Gu,et al.  Impact of hemicelluloses and pectin on sphere-like bacterial cellulose assembly , 2012 .

[30]  M. Schramm,et al.  Factors affecting production of cellulose at the air/liquid interface of a culture of Acetobacter xylinum. , 1954, Journal of general microbiology.

[31]  X. Perret,et al.  Proteome analysis of Acetobacter pasteurianus during acetic acid fermentation. , 2012, Journal of proteomics.

[32]  M. Gullo,et al.  Acetic Acid Bacteria: Physiology and Carbon Sources Oxidation , 2013, Indian Journal of Microbiology.

[33]  D. Kręgiel,et al.  Consortia formed by yeasts and acetic acid bacteria Asaia spp. in soft drinks , 2017, Antonie van Leeuwenhoek.

[34]  Fen Fen Zhang,et al.  Biodiversity of yeasts, lactic acid bacteria and acetic acid bacteria in the fermentation of "Shanxi aged vinegar", a traditional Chinese vinegar. , 2012, Food microbiology.

[35]  J. Guillamón,et al.  Application of molecular methods for routine identification of acetic acid bacteria. , 2006, International journal of food microbiology.

[36]  A. Terpou,et al.  Progress in bacterial cellulose matrices for biotechnological applications. , 2016, Bioresource technology.

[37]  M. Janaki Ramaiah,et al.  Antioxidant and anti-inflammatory levan produced from Acetobacter xylinum NCIM2526 and its statistical optimization. , 2015, Carbohydrate polymers.

[38]  S. Ribeiro,et al.  Draft Genome Sequence of Komagataeibacter intermedius Strain AF2, a Producer of Cellulose, Isolated from Kombucha Tea , 2015, Genome Announcements.

[39]  L. Hernández,et al.  Review of Levan polysaccharide: From a century of past experiences to future prospects. , 2016, Biotechnology advances.

[40]  Yang Chen,et al.  Correlation between ethanol resistance and characteristics of PQQ-dependent ADH in acetic acid bacteria , 2016, European Food Research and Technology.

[41]  Bin Wang,et al.  Overview on mechanisms of acetic acid resistance in acetic acid bacteria , 2015, World Journal of Microbiology and Biotechnology.

[42]  Paolo Giudici,et al.  Acetic acid bacteria in traditional balsamic vinegar: phenotypic traits relevant for starter cultures selection. , 2008, International journal of food microbiology.

[43]  M. Himmel,et al.  High-temperature behavior of cellulose I. , 2011, The journal of physical chemistry. B.

[44]  Albert Mas,et al.  Acetic Acid Bacteria and the Production and Quality of Wine Vinegar , 2014, TheScientificWorldJournal.

[45]  M. Schramm,et al.  Synthesis of cellulose by Acetobacter xylinum. II. Preparation of freeze-dried cells capable of polymerizing glucose to cellulose. , 1954, The Biochemical journal.

[46]  M. Teuber,et al.  Characterization of the microflora of high acid submerged vinegar fermenters by distinct plasmid profiles , 1987, Biotechnology Letters.

[47]  Yuguo Zheng,et al.  Production of 1,3-dihydroxyacetone from glycerol by Gluconobacter oxydans ZJB09112. , 2010, Journal of microbiology and biotechnology.

[48]  J. Guillamón,et al.  Population dynamics of acetic acid bacteria during traditional wine vinegar production. , 2010, International journal of food microbiology.

[49]  K. Matsushita,et al.  Purification and Properties of Particulate Alcohol Dehydrogenase from Acetobacter aceti , 1978 .

[50]  M. Rupnik,et al.  Diversity of the microbiota involved in wine and organic apple cider submerged vinegar production as revealed by DHPLC analysis and next-generation sequencing. , 2016, International journal of food microbiology.

[51]  K. Arima,et al.  Isolation and Identification of Acetic Acid Bacteria for Submerged Acetic Acid Fermentation at High Temperature , 1980 .

[52]  Cheng-Kang Lee,et al.  Utilization of acetate buffer to improve bacterial cellulose production by Gluconacetobacter xylinus , 2016 .

[53]  Y. Yamada,et al.  The phylogeny of acetic acid bacteria based on the partial sequences of 16S ribosomal RNA: the elevation of the subgenus Gluconoacetobacter to the generic level. , 1997, Bioscience, biotechnology, and biochemistry.

[54]  J. Moore,et al.  Asaia sp., an Unusual Spoilage Organism of Fruit-Flavored Bottled Water , 2002, Applied and Environmental Microbiology.

[55]  V. S. Moholkar,et al.  Optimization of 1,3-dihydroxyacetone production from crude glycerol by immobilized Gluconobacter oxydans MTCC 904. , 2016, Bioresource technology.

[56]  A. Ashori,et al.  Production of bacterial cellulose using different carbon sources and culture media. , 2015, Carbohydrate polymers.

[57]  M. Cirigliano,et al.  A Selective Medium for the Isolation and Differentiation of Gluconobacter and Acetobacter , 1982 .

[58]  M. Gullo,et al.  Characterization of acetic acid bacteria in "traditional balsamic vinegar". , 2006, International journal of food microbiology.

[59]  Ana M. Cañete-Rodríguez,et al.  Gluconic acid: Properties, production methods and applications-An excellent opportunity for agro-industrial by-products and waste bio-valorization , 2016 .

[60]  Duangjai Ochaikul,et al.  Subdivision of the genus Gluconacetobacter Yamada, Hoshino and Ishikawa 1998: the proposal of Komagatabacter gen. nov., for strains accommodated to the Gluconacetobacter xylinus group in the α-Proteobacteria , 2011, Annals of Microbiology.

[61]  S. T. Cowan Bergey's Manual of Determinative Bacteriology , 1948, Nature.

[62]  K. Matsushita,et al.  Biooxidation with PQQ‐ and FAD‐Dependent Dehydrogenases , 2007 .

[63]  W. Hammes,et al.  Description of a starter culture preparation for vinegar fermentation , 1997 .

[64]  Z. Guzel‐Seydim,et al.  Functional properties of vinegar. , 2014, Journal of food science.

[65]  J. Trček,et al.  Updates on quick identification of acetic acid bacteria with a focus on the 16S-23S rRNA gene internal transcribed spacer and the analysis of cell proteins by MALDI-TOF mass spectrometry. , 2015, International journal of food microbiology.

[66]  M. Tonolla,et al.  Rapid identification of acetic acid bacteria using MALDI-TOF mass spectrometry fingerprinting. , 2013, Systematic and applied microbiology.

[67]  C. Torres,et al.  Rapid molecular methods for enumeration and taxonomical identification of acetic acid bacteria responsible for submerged vinegar production , 2010 .

[68]  Ahmet E Yetiman,et al.  Identification of acetic acid bacteria in traditionally produced vinegar and mother of vinegar by using different molecular techniques. , 2015, International journal of food microbiology.

[69]  C. G. Edwards,et al.  Wine Microbiology: Practical Applications and Procedures , 1997 .

[70]  Nho-Eul Song,et al.  Microbial community, and biochemical and physiological properties of Korean traditional black raspberry (Robus coreanus Miquel) vinegar. , 2016, Journal of the science of food and agriculture.

[71]  K. Matsushita,et al.  Alcohol dehydrogenase of acetic acid bacteria: structure, mode of action, and applications in biotechnology , 2010, Applied Microbiology and Biotechnology.

[72]  Yuzo Yamada,et al.  Distribution of Ubiquinone 10 and 9 in Acetic Acid Bacteria and Its Relation to the Classification of Genera Gluconobacter and Acetobacter, Especially of So-called Intermediate Strains , 1968 .

[73]  J. P. Dijken,et al.  Role of NADP-dependent andquinoprotein glucose dehydrogenases ingluconic acid production byGluconobacter oxydans , 1989 .

[74]  Inés María Santos-Dueñas,et al.  Rapid method for total, viable and non-viable acetic acid bacteria determination during acetification process , 2006 .

[75]  Yue Zhang,et al.  Utilization of bacterial cellulose in food , 2014 .

[76]  K. Matsushita,et al.  Purification and Characterization of Particulate Alcohol Dehydrogenase from Gluconobacter suboxydans , 1978 .

[77]  Yuzo Yamada,et al.  Genera and species in acetic acid bacteria. , 2008, International journal of food microbiology.

[78]  G. Cho,et al.  Complete Genome Sequences of Two Acetic Acid-Producing Acetobacter pasteurianus Strains (Subsp. ascendens LMG 1590T and Subsp. paradoxus LMG 1591T) , 2017, Front. Bioeng. Biotechnol..

[79]  L. Gibson The hierarchical structure and mechanics of plant materials , 2012, Journal of The Royal Society Interface.

[80]  M. Hamdi,et al.  Development of a beverage from red grape juice fermented with the Kombucha consortium , 2016, Annals of Microbiology.

[81]  U. Deppenmeier,et al.  Biochemistry and biotechnological applications of Gluconobacter strains , 2002, Applied Microbiology and Biotechnology.

[82]  Hiroshi Horikawa,et al.  Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus , 2009, Nucleic acids research.

[83]  Ken-ichiro Suzuki,et al.  ACETOBACTER POLYOXOGENES SP. NOV., A NEW SPECIES OF AN ACETIC ACID BACTERIUM USEFUL FOR PRODUCING VINEGAR WITH HIGH ACIDITY , 1985 .

[84]  S. Valla,et al.  Cellulose-negative Mutants of Acetobacter xylinum , 1982 .

[85]  I. Sengun,et al.  Importance of acetic acid bacteria in food industry , 2011 .

[86]  J. Guillamón,et al.  Identification and quantification of acetic acid bacteria in wine and vinegar by TaqMan-MGB probes. , 2010, Food microbiology.

[87]  P. H. Le,et al.  Screening the optimal ratio of symbiosis between isolated yeast and acetic acid bacteria strain from traditional kombucha for high-level production of glucuronic acid , 2015 .

[88]  L. De Vero,et al.  Genus-specific profile of acetic acid bacteria by 16S rDNA PCR-DGGE. , 2008, International journal of food microbiology.

[89]  Elena Verzelloni,et al.  Aerobic submerged fermentation by acetic acid bacteria for vinegar production: Process and biotechnological aspects , 2014 .

[90]  G. Leonard,et al.  Design, Development, and Use of Molecular Primers and Probes for the Detection of Gluconacetobacter Species in the Pink Sugarcane Mealybug , 2005, Microbial Ecology.

[91]  I. Ohad,et al.  SYNTHESIS OF CELLULOSE BY ACETOBACTER XYLINUM , 1965, The Journal of cell biology.

[92]  P. Raspor,et al.  Biotechnological applications of acetic acid bacteria. , 2008, Critical reviews in biotechnology.

[93]  E. Mateo,et al.  Comparison of D-gluconic acid production in selected strains of acetic acid bacteria. , 2016, International journal of food microbiology.

[94]  P. de Vos,et al.  Acetobacter ghanensis sp. nov., a novel acetic acid bacterium isolated from traditional heap fermentations of Ghanaian cocoa beans. , 2007, International journal of systematic and evolutionary microbiology.

[95]  P. de Vos,et al.  Differentiation of species of the family Acetobacteraceae by AFLP DNA fingerprinting: Gluconacetobacter kombuchae is a later heterotypic synonym of Gluconacetobacter hansenii. , 2009, International journal of systematic and evolutionary microbiology.

[96]  E. Bartowsky,et al.  Acetic acid bacteria spoilage of bottled red wine -- a review. , 2008, International journal of food microbiology.