Heterologous Expression of Argininosuccinate Synthase From Oenococcus oeni Enhances the Acid Resistance of Lactobacillus plantarum

Oenococcus oeni can survive well in wine (an acid-stress environment) and dominate malolactic fermentation (MLF). To demonstrate a possible role of argininosuccinate synthase gene (argG) in the acid tolerance response of O. oeni, a related argG gene was inserted into a plasmid pMG36e and heterologously expressed in Lactobacillus plantarum SL09, a wine isolate belonging to a species of relevant importance in MLF. The expression levels of the argG gene in L. plantarum were analyzed by RT-qPCR, argininosuccinate synthase (ASS) activity and cell properties (amino acids, pH, H+-ATPase activity, and ATP levels) were determined at pH 3.7 in comparison with that at pH 6.3. Results showed that the recombinant strain L. plantarum SL09 (pMG36eargG) exhibited stronger growth performance compared with the control strain (without argG gene), and the expression levels of hsp1, cfa, atp, the citrate and malate metabolic genes were apparently increased under acid stress. In addition, the recombinant strain exhibited 11.0-, 2.0-, 1.9-fold higher ASS activity, H+-ATPase activity and intracellular ATP level, compared with the corresponding values for control strain during acid-stresses condition, which may take responsible for the acid tolerance enhancement of the recombinant strain. This is the first work report on heterologous expression of argG gene, and the results presented in this study will be beneficial for the research on acid stress response of O. oeni.

[1]  A. Rieu,et al.  The Phenotypic Analysis of Lactobacillus plantarum shsp Mutants Reveals a Potential Role for hsp1 in Cryotolerance , 2019, Front. Microbiol..

[2]  P. Lucas,et al.  Distribution of Oenococcus oeni populations in natural habitats , 2019, Applied Microbiology and Biotechnology.

[3]  T. Msadek,et al.  CtsR, the Master Regulator of Stress-Response in Oenococcus oeni, Is a Heat Sensor Interacting With ClpL1 , 2018, Front. Microbiol..

[4]  M. Dimopoulou,et al.  Oenococcus oeni Exopolysaccharide Biosynthesis, a Tool to Improve Malolactic Starter Performance , 2018, Front. Microbiol..

[5]  Hua Li,et al.  Selection and Validation of Reference Genes for Quantitative Real-Time PCR Normalization Under Ethanol Stress Conditions in Oenococcus oeni SD-2a , 2018, Front. Microbiol..

[6]  J. Romero,et al.  Oenococcus oeni in Chilean Red Wines: Technological and Genomic Characterization , 2018, Front. Microbiol..

[7]  Jing Su,et al.  Transcriptomic Analysis of Oenococcus oeni SD-2a Response to Acid Shock by RNA-Seq , 2017, Front. Microbiol..

[8]  A. Rieu,et al.  Production of the small heat shock protein Lo18 from Oenococcus oeni in Lactococcus lactis improves its stress tolerance. , 2017, International journal of food microbiology.

[9]  C. Li,et al.  Molecular mechanisms and in vitro antioxidant effects of Lactobacillus plantarum MA2. , 2017, Food chemistry.

[10]  A. Bordons,et al.  Transcriptomic and Proteomic Analysis of Oenococcus oeni Adaptation to Wine Stress Conditions , 2016, Front. Microbiol..

[11]  Wenjun Liu,et al.  Isolation and Identification of Lactic Acid Bacteria from Traditional Dairy Products in Baotou and Bayannur of Midwestern Inner Mongolia and q-PCR Analysis of Predominant Species , 2016, Korean journal for food science of animal resources.

[12]  P. Russo,et al.  Technological properties of Lactobacillus plantarum strains isolated from grape must fermentation. , 2016, Food microbiology.

[13]  M. Kleerebezem,et al.  Stress Physiology of Lactic Acid Bacteria , 2016, Microbiology and Molecular Reviews.

[14]  Mario Aranda,et al.  Identification of biogenic amines-producing lactic acid bacteria isolated from spontaneous malolactic fermentation of chilean red wines , 2016 .

[15]  Jinhwan Lee,et al.  Uncultured bacterial diversity in a seawater recirculating aquaculture system revealed by 16S rRNA gene amplicon sequencing , 2016, Journal of Microbiology.

[16]  T. Msadek,et al.  The Antisense RNA Approach: a New Application for In Vivo Investigation of the Stress Response of Oenococcus oeni, a Wine-Associated Lactic Acid Bacterium , 2015, Applied and Environmental Microbiology.

[17]  P. Grbin,et al.  Improving Oenococcus oeni to overcome challenges of wine malolactic fermentation. , 2015, Trends in biotechnology.

[18]  M. Constantí,et al.  Arginine deiminase pathway genes and arginine degradation variability in Oenococcus oeni strains , 2015, Folia Microbiologica.

[19]  Jing Su,et al.  Multilocus sequence typing and pulsed-field gel electrophoresis analysis of Oenococcus oeni from different wine-producing regions of China. , 2015, International journal of food microbiology.

[20]  L. Delfederico,et al.  Prevalence of Lactobacillus plantarum and Oenococcus oeni during spontaneous malolactic fermentation in Patagonian red wines revealed by polymerase chain reaction-denaturing gradient gel electrophoresis with two targeted genes , 2015 .

[21]  Yahong Yuan,et al.  Ultrasensitive and simultaneous determination of twenty-one amino acids and amines in culture media, red wine and beer. , 2014, Food chemistry.

[22]  J. Covès,et al.  Adaptation of the Wine Bacterium Oenococcus oeni to Ethanol Stress: Role of the Small Heat Shock Protein Lo18 in Membrane Integrity , 2014, Applied and Environmental Microbiology.

[23]  P. R. Jensen,et al.  Engineering strategies aimed at control of acidification rate of lactic acid bacteria. , 2013, Current opinion in biotechnology.

[24]  G. Mathiesen,et al.  Heterologous expression of Oenococcus oeni malolactic enzyme in Lactobacillus plantarum for improved malolactic fermentation , 2012, AMB Express.

[25]  P. Russo,et al.  Biogenic Amines Degradation by Lactobacillus plantarum: Toward a Potential Application in Wine , 2012, Front. Microbio..

[26]  Yuriy Rebets,et al.  SimReg1 is a master switch for biosynthesis and export of simocyclinone D8 and its precursors , 2012, AMB Express.

[27]  S. Krieger-Weber,et al.  Lactobacillus: the Next Generation of Malolactic Fermentation Starter Cultures—an Overview , 2011 .

[28]  J. Guzzo Stress Responses of Oenococcus oeni , 2011 .

[29]  A. Bordons,et al.  Multigenic expression analysis as an approach to understanding the behaviour of Oenococcus oeni in wine-like conditions. , 2010, International journal of food microbiology.

[30]  R. Duary,et al.  Expression of the atpD gene in probiotic Lactobacillus plantarum strains under in vitro acidic conditions using RT-qPCR. , 2010, Research in microbiology.

[31]  M. Maiden,et al.  Multilocus sequence typing. , 2009, Methods in molecular biology.

[32]  H. Alexandre,et al.  An improved protocol for electroporation of Oenococcus oeni ATCC BAA‐1163 using ethanol as immediate membrane fluidizing agent , 2008, Letters in applied microbiology.

[33]  S. Chu-Ky,et al.  Changes in membrane lipid composition in ethanol- and acid-adapted Oenococcus oeni cells: characterization of the cfa gene by heterologous complementation. , 2008, Microbiology.

[34]  G. Spano,et al.  Validation of an internal control gene to apply reverse transcription quantitative PCR to study heat, cold and ethanol stresses in Lactobacillus plantarum , 2008 .

[35]  J. Hugenholtz,et al.  Glutathione Protects Lactococcus lactis against Acid Stress , 2007, Applied and Environmental Microbiology.

[36]  F. Remize,et al.  Dual effect of organic acids as a function of external pH in Oenococcus oeni , 2007, Archives of Microbiology.

[37]  Per Ambus,et al.  Enzymatic Evidence for the Key Role of Arginine in Nitrogen Translocation by Arbuscular Mycorrhizal Fungi1[OA] , 2006, Plant Physiology.

[38]  J. Bourdineaud Both arginine and fructose stimulate pH-independent resistance in the wine bacteria Oenococcus oeni. , 2006, International journal of food microbiology.

[39]  M. Zúñiga,et al.  Amino Acid Catabolic Pathways of Lactic Acid Bacteria , 2006, Critical reviews in microbiology.

[40]  M. C. Manca de Nadra,et al.  Influence of ethanol and low pH on arginine and citrulline metabolism in lactic acid bacteria from wine. , 2005, Research in microbiology.

[41]  D. Garmyn,et al.  A new vector, pGID052, for genetic transfer in Oenococcus oeni. , 2004, FEMS microbiology letters.

[42]  G. Fia,et al.  Influence of different pH values and inoculation time on the growth and malolactic activity of a strain of Oenococcus oeni , 2003 .

[43]  B. Lee,et al.  Induction of Oenococcus oeni H+-ATPase activity and mRNA transcription under acidic conditions. , 2003, FEMS microbiology letters.

[44]  A. Lonvaud-Funel,et al.  L' arginine stimule la preadaptation au vin chez la bacterie Oenococcus oeni. , 2002 .

[45]  P. Howell,et al.  Substrate Induced Conformational Changes in Argininosuccinate Synthetase* , 2002, The Journal of Biological Chemistry.

[46]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[47]  T. Tonon,et al.  The arcABC gene cluster encoding the arginine deiminase pathway of Oenococcus oeni, and arginine induction of a CRP-like gene. , 2001, Research in microbiology.

[48]  T. Tonon,et al.  Metabolism of arginine and its positive effect on growth and revival of Oenococcus oeni , 2000, Journal of applied microbiology.

[49]  R. Quivey,et al.  Adaptation of oral streptococci to low pH. , 2000, Advances in microbial physiology.

[50]  E. O'Sullivan,et al.  Relationship between Acid Tolerance, Cytoplasmic pH, and ATP and H+-ATPase Levels in Chemostat Cultures of Lactococcus lactis , 1999, Applied and Environmental Microbiology.

[51]  K. Fearon,et al.  31P NMR spectroscopy in oligonucleotide research and development. , 1997, Antisense & nucleic acid drug development.

[52]  M. Bagby Products from Vegetable Oils: Two Examples , 1996 .

[53]  C. Stevens,et al.  Aquaporin 4 and glymphatic flow have central roles in brain fluid homeostasis , 2021, Nature Reviews Neuroscience.