Actinobacillus succinogenes: Advances on succinic acid production and prospects for development of integrated biorefineries

Abstract Actinobacillus succinogenes is a wild-type bacterial strain, isolated from bovine rumen, known as one of the most efficient natural producers of succinic acid. Herein, the factors contributing to the fermentative production of succinic acid by A. succinogenes are reviewed with particular focus on raw materials, culture conditions, significance of carbon dioxide availability and downstream separation and purification. The metabolic potential of this strain is evaluated through discussion of the pathways involved in succinic acid production, genome analysis as well as the development of A. succinogenes mutants. The review also addresses the importance of by-product formation during fermentation that constitutes an important aspect regulating succinic acid production by A. succinogenes. The prospect of integrating succinic acid production in future biorefineries is assessed.

[1]  K. Jantama,et al.  Production of succinic acid from sucrose and sugarcane molasses by metabolically engineered Escherichia coli. , 2012, Bioresource technology.

[2]  Alvaro Orjuela,et al.  A novel process for recovery of fermentation-derived succinic acid , 2011 .

[3]  J. Gregory Zeikus,et al.  Insights into Actinobacillus succinogenes Fermentative Metabolism in a Chemically Defined Growth Medium , 2005, Applied and Environmental Microbiology.

[4]  M. Jain,et al.  Actinobacillus succinogenes sp. nov., a novel succinic-acid-producing strain from the bovine rumen. , 1999, International journal of systematic bacteriology.

[5]  Masayuki Inui,et al.  An efficient succinic acid production process in a metabolically engineered Corynebacterium glutamicum strain , 2008, Applied Microbiology and Biotechnology.

[6]  N P Nghiem,et al.  Production of succinic acid by anaerobiospirillum succiniciproducens , 1997, Applied biochemistry and biotechnology.

[7]  Eleni Vasilakou,et al.  Laminaria digitata as a potential carbon source for succinic acid and bioenergy production in a biorefinery perspective , 2015 .

[8]  W. Nicol,et al.  Continuous succinic acid fermentation by Actinobacillus succinogenes , 2013 .

[9]  Y. Ni,et al.  Succinic acid production from corn stover by simultaneous saccharification and fermentation using Actinobacillus succinogenes. , 2010, Bioresource technology.

[10]  J. Zeikus,et al.  Microbial Utilization of Electrically Reduced Neutral Red as the Sole Electron Donor for Growth and Metabolite Production , 1999, Applied and Environmental Microbiology.

[11]  Simon Perry,et al.  Implementation of Heat Integration to Improve the Sustainability of an Integrated Biodiesel Biorefinery , 2012 .

[12]  S. Papanikolaou,et al.  Integrated sunflower-based biorefinery for the production of antioxidants, protein isolate and poly(3-hydroxybutyrate) , 2015 .

[13]  Y. Ni,et al.  Fermentative production of succinic acid from straw hydrolysate by Actinobacillus succinogenes. , 2009, Bioresource technology.

[14]  Min Jiang,et al.  A complete industrial system for economical succinic acid production by Actinobacillus succinogenes. , 2011, Bioresource technology.

[15]  Q. Yan,et al.  Fermentation process for continuous production of succinic acid in a fibrous bed bioreactor , 2014 .

[16]  Lei-Lei Zhu,et al.  Economical succinic acid production from cane molasses by Actinobacillus succinogenes. , 2008, Bioresource technology.

[17]  Giuseppe Mazza,et al.  Lignin in straw of herbaceous crops , 2008 .

[18]  Jan Springer,et al.  From the Sugar Platform to biofuels and biochemicals : Final report for the European Commission Directorate-General Energy , 2015 .

[19]  Hong-Mei Li,et al.  Significance of CO2 donor on the production of succinic acid by Actinobacillus succinogenes ATCC 55618 , 2011, Microbial cell factories.

[20]  Min Jiang,et al.  Succinic Acid Production by Actinobacillus succinogenes Using Spent Brewer's Yeast Hydrolysate as a Nitrogen Source , 2010, Applied biochemistry and biotechnology.

[21]  Zhi-hao Sun,et al.  Enhanced succinic acid production by Actinobacillus succinogenes after genome shuffling , 2013, Journal of Industrial Microbiology & Biotechnology.

[22]  John A Posada,et al.  Design and analysis of biorefineries based on raw glycerol: addressing the glycerol problem. , 2012, Bioresource technology.

[23]  P. Wei,et al.  Ultrasonic pretreatment and acid hydrolysis of sugarcane bagasse for succinic acid production using Actinobacillus succinogenes , 2013, Bioprocess and Biosystems Engineering.

[24]  Jeong Wook Lee,et al.  Systems metabolic engineering of microorganisms for natural and non-natural chemicals. , 2012, Nature chemical biology.

[25]  P. Wei,et al.  Enhancement of succinic acid production by osmotic-tolerant mutant strain of Actinobacillus succinogenes , 2011 .

[26]  Wim Soetaert,et al.  Microbial succinic acid production: Natural versus metabolic engineered producers , 2010 .

[27]  C. Vieille,et al.  13C-metabolic flux analysis of Actinobacillus succinogenes fermentative metabolism at different NaHCO3 and H2 concentrations. , 2008, Metabolic engineering.

[28]  Joseph J. Bozell,et al.  Technology development for the production of biobased products from biorefinery carbohydrates—the US Department of Energy’s “Top 10” revisited , 2010 .

[29]  J. Zeikus,et al.  Utilization of Electrically Reduced Neutral Red byActinobacillus succinogenes: Physiological Function of Neutral Red in Membrane-Driven Fumarate Reduction and Energy Conservation , 1999, Journal of bacteriology.

[30]  M. Eiteman,et al.  Succinate production in dual-phase Escherichia coli fermentations depends on the time of transition from aerobic to anaerobic conditions , 2002, Journal of Industrial Microbiology and Biotechnology.

[31]  P. Wei,et al.  Isolation of NH₄+-tolerant mutants of Actinobacillus succinogenes for succinic acid production by continuous selection. , 2010, Journal of microbiology and biotechnology.

[32]  Jianmin Xing,et al.  Efficient conversion of crop stalk wastes into succinic acid production by Actinobacillus succinogenes. , 2010, Bioresource technology.

[33]  Colin Webb,et al.  Substrate and product inhibition kinetics in succinic acid production by Actinobacillus succinogenes , 2008 .

[34]  Ulf Sonesson,et al.  The methodology of the FAO study: Global Food Losses and Food Waste - extent, causes and prevention”- FAO, 2011 , 2013 .

[35]  Qiang Yan,et al.  A fibrous bed bioreactor to improve the productivity of succinic acid by Actinobacillus succinogenes , 2014 .

[36]  Y. Jun,et al.  Kinetic study for the extraction of succinic acid with TOA in fermentation broth; effects of pH, salt and contaminated acid , 2007 .

[37]  M. Zhang,et al.  Succinic acid production from sucrose by Actinobacillus succinogenes NJ113. , 2014, Bioresource technology.

[38]  S. Papanikolaou,et al.  Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. , 2014, Chemical Society reviews.

[39]  E. Padan.  Functional and structural dynamics of NhaA, a prototype for Na(+) and H(+) antiporters, which are responsible for Na(+) and H(+) homeostasis in cells. , 2014, Biochimica et biophysica acta.

[40]  Abolghasem Shahbazi,et al.  Succinic Acid Production from Cheese Whey using Actinobacillus succinogenes 130 Z , 2008, Applied biochemistry and biotechnology.

[41]  Rafael Luque,et al.  Towards a bio-based industry: benign catalytic esterifications of succinic acid in the presence of water. , 2007, Chemistry.

[42]  S. Lee,et al.  Systems strategies for developing industrial microbial strains , 2015, Nature Biotechnology.

[43]  S. Lee,et al.  Production of succinic acid by bacterial fermentation , 2006 .

[44]  Min Jiang,et al.  Succinic acid production by Actinobacillus succinogenes NJ113 using corn steep liquor powder as nitrogen source. , 2013, Bioresource technology.

[45]  V. González-Álvarez,et al.  Succinic Acid Production with Actinobacillus succinogenes ZT-130 in the Presence of Succinic Acid , 2009, Current Microbiology.

[46]  C. Du,et al.  Novel resin-based vacuum distillation-crystallisation method for recovery of succinic acid crystals from fermentation broths , 2010 .

[47]  Colin Webb,et al.  Wheat‐based biorefining strategy for fermentative production and chemical transformations of succinic acid , 2012 .

[48]  W. Nicol,et al.  Continuous succinic acid production by Actinobacillus succinogenes in a biofilm reactor: Steady-state metabolic flux variation , 2014 .

[49]  Xueli Gao,et al.  Preparation of succinic acid using bipolar membrane electrodialysis , 2014 .

[50]  J. Zeikus,et al.  Influence of CO2-HCO3− Levels and pH on Growth, Succinate Production, and Enzyme Activities of Anaerobiospirillum succiniciproducens , 1991, Applied and environmental microbiology.

[51]  J. Zeikus,et al.  Whey Fermentation by Anaerobiospirillum succiniciproducens for Production of a Succinate-Based Animal Feed Additive , 1999, Applied and Environmental Microbiology.

[52]  Alicia Clum,et al.  A genomic perspective on the potential of Actinobacillus succinogenes for industrial succinate production , 2010, BMC Genomics.

[53]  Ya-Jie Tang,et al.  Performance analyses of a neutralizing agent combination strategy for the production of succinic acid by Actinobacillus succinogenes ATCC 55618 , 2012, Bioprocess and Biosystems Engineering.

[54]  Jing Zeng,et al.  Improved Succinate Production by Metabolic Engineering , 2013, BioMed research international.

[55]  Sang Yup Lee,et al.  The genome sequence of the capnophilic rumen bacterium Mannheimia succiniciproducens , 2004, Nature Biotechnology.

[56]  Baohua Guo,et al.  Novel membrane-based biotechnological alternative process for succinic acid production and chemical synthesis of bio-based poly (butylene succinate). , 2014, Bioresource technology.

[57]  Sang Yup Lee,et al.  Batch and continuous fermentation of succinic acid from wood hydrolysate by Mannheimia succiniciproducens MBEL55E , 2004 .

[58]  Jianmin Xing,et al.  Efficient production of succinic acid from corn stalk hydrolysates by a recombinant Escherichia coli with ptsG mutation , 2011 .

[59]  Min Jiang,et al.  Effect of redox potential regulation on succinic acid production by Actinobacillus succinogenes , 2010, Bioprocess and biosystems engineering.

[60]  Byung Hong Kim,et al.  Insight into Biomass as a Renewable Carbon Source for the Production of Succinic Acid and the Factors Affecting the Metabolic Flux toward Higher Succinate Yield , 2014 .

[61]  D. Weuster‐Botz,et al.  New reactive extraction systems for separation of bio-succinic acid , 2011, Bioprocess and biosystems engineering.

[62]  P. Wei,et al.  Succinic acid production from cellobiose by Actinobacillus succinogenes. , 2013, Bioresource technology.

[63]  Hyohak Song,et al.  Genome-Based Metabolic Engineering of Mannheimia succiniciproducens for Succinic Acid Production , 2006, Applied and Environmental Microbiology.

[64]  P. Wei,et al.  Influence of Osmotic Stress on Fermentative Production of Succinic Acid by Actinobacillus succinogenes , 2011, Applied biochemistry and biotechnology.

[65]  Xuebing Zhao,et al.  Biotechnological production of succinic acid: current state and perspectives , 2012 .

[66]  Martin Kumar Patel,et al.  Succinic acid production derived from carbohydrates: An energy and greenhouse gas assessment of a platform chemical toward a bio‐based economy , 2014 .

[67]  P. Wei,et al.  Effect of biotin and a similar compound on succinic acid fermentation by Actinobacillus succinogenes in a chemically defined medium , 2012 .

[68]  Efstratios N. Pistikopoulos,et al.  Bioprocess systems engineering: transferring traditional process engineering principles to industrial biotechnology , 2012, Computational and structural biotechnology journal.

[69]  D. R. Raman,et al.  Development and validation of a technoeconomic analysis tool for early-stage evaluation of bio-based chemical production processes. , 2013, Bioresource technology.

[70]  Paul M. Rose,et al.  The fractionation of valuable wax products from wheat straw using CO2 , 2006 .

[71]  Colin Webb,et al.  Glycerol utilisation for the production of chemicals: conversion to succinic acid, a combined experimental and computational study. , 2011 .

[72]  W. V. van Gulik,et al.  Towards large scale fermentative production of succinic acid. , 2014, Current opinion in biotechnology.

[73]  G. Centi,et al.  Carbon dioxide recycling: emerging large-scale technologies with industrial potential. , 2011, ChemSusChem.

[74]  Christoph Wittmann,et al.  Systems‐wide analysis and engineering of metabolic pathway fluxes in bio‐succinate producing Basfia succiniciproducens , 2013, Biotechnology and bioengineering.

[75]  Z. Su,et al.  Integrated bioprocess for high-efficiency production of succinic acid in an expanded-bed adsorption system , 2011 .

[76]  Y. Ni,et al.  Strategies of pH control and glucose‐fed batch fermentation for production of succinic acid by Actinobacillus succinogenes CGMCC1593 , 2008 .

[77]  P. Freestone,et al.  Calcium signalling in bacteria , 1996, Journal of bacteriology.

[78]  H. Chang,et al.  Effects of medium components on the growth of Anaerobiospirillum succiniciproducens and succinic acid production , 1999 .

[79]  Honghua Jia,et al.  Succinic acid production from sucrose and molasses by metabolically engineered E. coli using a cell surface display system , 2014 .

[80]  S. P. Sineoky,et al.  Production of succinic acid at low pH by a recombinant strain of the aerobic yeast Yarrowia lipolytica , 2010, Biotechnology and bioengineering.

[81]  Colin Webb,et al.  A techno-economic analysis of biodiesel biorefineries: Assessment of integrated designs for the co-production of fuels and chemicals , 2011 .

[82]  Colin Webb,et al.  Cereal-based biorefinery development: utilisation of wheat milling by-products for the production of succinic acid. , 2009, Journal of biotechnology.

[83]  Charles Jackson,et al.  Toward an integrated straw‐based biorefinery , 2007 .

[84]  A. Idris,et al.  Recent advances in production of succinic acid from lignocellulosic biomass , 2013, Applied Microbiology and Biotechnology.

[85]  Ioannis K. Kookos,et al.  Wine lees valorization: Biorefinery development including production of a generic fermentation feedstock employed for poly(3-hydroxybutyrate) synthesis , 2015 .

[86]  F. Gao,et al.  Efficient decolorization and deproteinization using uniform polymer microspheres in the succinic acid biorefinery from bio-waste cotton (Gossypium hirsutum L.) stalks. , 2013, Bioresource technology.

[87]  S. B. Sawant,et al.  Reduction of Maleic Acid to Succinic Acid on Titanium Cathode , 2004 .

[88]  Víctor González-Álvarez,et al.  Kinetic study of succinic acid production by Actinobacillus succinogenes ZT-130 , 2008 .

[89]  Xueli Zhang,et al.  Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate , 2008, Biotechnology and bioengineering.

[90]  G. Bennett,et al.  Succinate production in Escherichia coli , 2012, Biotechnology journal.

[91]  H. Chang,et al.  Batch and continuous cultures of Mannheimia succiniciproducens MBEL55E for the production of succinic acid from whey and corn steep liquor , 2003, Bioprocess and biosystems engineering.

[92]  Sang Yup Lee,et al.  Effective purification of succinic acid from fermentation broth produced by Mannheimia succiniciproducens , 2006 .

[93]  D. Weuster‐Botz,et al.  Esterification of bio-based succinic acid in biphasic systems: Comparison of chemical and biological catalysts , 2012 .

[94]  H. Chang,et al.  Succinic acid production by Anaerobiospirillum succiniciproducens ATCC 29305 growing on galactose, galactose/glucose, and galactose/lactose. , 2008, Journal of microbiology and biotechnology.

[95]  Qin Ye,et al.  Development of succinic acid production from corncob hydrolysate by Actinobacillus succinogenes , 2010, Journal of Industrial Microbiology & Biotechnology.

[96]  J. Clark,et al.  Tunable mesoporous materials optimised for aqueous phase esterifications , 2007 .

[97]  P. Wei,et al.  CO2 fixation for succinic acid production by engineered Escherichia coli co-expressing pyruvate carboxylase and nicotinic acid phosphoribosyltransferase , 2013 .

[98]  Longan Shang,et al.  Enhanced production of succinic acid by Actinobacillus succinogenes with reductive carbon source , 2010 .

[99]  L. Prasad,et al.  Structure of PEP carboxykinase from the succinate-producing Actinobacillus succinogenes: a new conserved active-site motif. , 2005, Acta crystallographica. Section D, Biological crystallography.

[100]  Jeong Wook Lee,et al.  Construction and Characterization of Shuttle Vectors for Succinic Acid-Producing Rumen Bacteria , 2007, Applied and Environmental Microbiology.

[101]  Min Jiang,et al.  Succinic Acid Production from Acid Hydrolysate of Corn Fiber by Actinobacillus succinogenes , 2010, Applied biochemistry and biotechnology.

[102]  Ulrika Rova,et al.  Detoxification requirements for bioconversion of softwood dilute acid hydrolyzates to succinic acid , 2009 .

[103]  A. Straathof,et al.  Techno-economic analysis of succinic acid production using adsorption from fermentation medium. , 2013 .

[104]  Ribo Huang,et al.  Optimization of succinic acid production from cane molasses by Actinobacillus succinogenes GXAS137 using response surface methodology (RSM) , 2014, Food Science and Biotechnology.

[105]  M. Xian,et al.  Fermentative Succinate Production: An Emerging Technology to Replace the Traditional Petrochemical Processes , 2013, BioMed research international.

[106]  Yair Shachar-Hill,et al.  Determining Actinobacillus succinogenes metabolic pathways and fluxes by NMR and GC-MS analyses of 13C-labeled metabolic product isotopomers. , 2007, Metabolic engineering.

[107]  Kequan Chen,et al.  Simultaneous saccharification and fermentation of acid-pretreated rapeseed meal for succinic acid production using Actinobacillus succinogenes. , 2011, Enzyme and microbial technology.

[108]  S. Papanikolaou,et al.  Extraction of phenolic compounds and succinic acid production from spent sulphite liquor , 2016 .

[109]  Min Jiang,et al.  Optimization of culture conditions in CO2 fixation for succinic acid production using Actinobacillus succinogenes , 2011, Journal of Industrial Microbiology & Biotechnology.

[110]  Xuebing Zhao,et al.  Downstream processing of biotechnological produced succinic acid , 2012, Applied Microbiology and Biotechnology.

[111]  J. Clark,et al.  Chemical transformations of succinic acid recovered from fermentation broths by a novel direct vacuum distillation-crystallisation method , 2009 .

[112]  H. Chang,et al.  Strategies for efficient repetitive production of succinate using metabolically engineered Escherichia coli , 2011, Bioprocess and biosystems engineering.

[113]  N. Pereira,et al.  Succinic acid production from sugarcane bagasse hemicellulose hydrolysate by Actinobacillus succinogenes , 2011, Journal of Industrial Microbiology & Biotechnology.

[114]  Dennis J. Miller,et al.  A novel process for recovery of fermentation-derived succinic acid: process design and economic analysis. , 2013, Bioresource technology.

[115]  C. Vieille,et al.  Construction of a shuttle vector for the overexpression of recombinant proteins in Actinobacillus succinogenes. , 2004, Plasmid.

[116]  M. Jiang,et al.  Enhanced Succinic Acid Production from Sake Lees Hydrolysate by Dilute Sulfuric Acid Pretreatment and Biotin Supplementation , 2012 .

[117]  Maria A M Reis,et al.  Succinic acid production from glycerol by Actinobacillus succinogenes using dimethylsulfoxide as electron acceptor. , 2014, New biotechnology.

[118]  Alan A. DiSpirito,et al.  Evaluation of succinic acid continuous and repeat-batch biofilm fermentation by Actinobacillus succinogenes using plastic composite support bioreactors , 2004, Applied Microbiology and Biotechnology.

[119]  Carol Sze Ki Lin,et al.  Utilisation of waste bread for fermentative succinic acid production , 2012 .

[120]  K. Blok,et al.  Producing bio-based bulk chemicals using industrial biotechnology saves energy and combats climate change. , 2007, Environmental science & technology.

[121]  P. Wei,et al.  Effects of overexpression of NAPRTase, NAMNAT, and NAD synthetase in the NAD(H) biosynthetic pathways on the NAD(H) pool, NADH/NAD+ ratio, and succinic acid production with different carbon sources by metabolically engineered Escherichia coli , 2013 .

[122]  Z. Su,et al.  Kinetic evaluation of products inhibition to succinic acid producers Escherichia coli NZN111, AFP111, BL21, and Actinobacillus succinogenes 130ZT , 2010, The Journal of Microbiology.