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References

  1. Tanasupawat S, Thongsanit J, Okada S, Komagata K. 2002. Lactic acid bacteria isolated from soy sauce mash in Thailand. J. Gen. Appl. Microbiol. 48: 201-209.
    Pubmed CrossRef
  2. Hanagata H, Shida O, Takagi H. 2003. Taxonomic homogeneity of a salt-tolerant lactic acid bacteria isolated from shoyu mash. J. Gen. Appl. Microbiol. 49: 95-100.
    Pubmed CrossRef
  3. Wu C D, Liu C L, He GQ, Huang J, Zhou RQ. 2013. Characterization of a multiple-stress tolerance Tetragenococcus halophilus and application as starter culture in Chinese Horsebean-Chili-Paste manufacture for quality improvement. Food Sci. Technol. Res. 19: 855-864.
    CrossRef
  4. Cui RY, Zheng J, Wu CD, Zhou RQ. 2014. Effect of different halophilic microbial fermentation patterns on the volatile compound profiles and sensory properties of soy sauce moromi. Eur. Food Res. Technol. 239: 321-331.
    CrossRef
  5. Roling W, Van Verseveld H. 1996. Characterization of Tetragenococcus halophila populations in indonesian soy mash (Kecap) fermentation. Appl. Environ. Microb. 62: 1203-1207.
    Pubmed PMC
  6. Udomsil N, Rodtong S, Choi YJ, Hua Y, Yongsawatdigul J. 2011. Use of Tetragenococcus halophilus as a starter culture for flavor improvement in fish sauce fermentation. J. Agr. Food Chem. 59: 8401-8408.
    Pubmed CrossRef
  7. Hahne H, Mäder U, Otto A, Bonn F, Steil L, Bremer E, et al. 2010. A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J. Bacteriol. 192: 870-882.
    Pubmed PMC CrossRef
  8. Kilstrup M, Jacobsen S, Hammer K, Vogensen FK. 1997. Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl. Environ. Microb. 63:1826-1837.
    Pubmed PMC
  9. Beales N. 2004. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Compr. Rev. Food Sci. Food 3: 1-20.
    CrossRef
  10. Diamant S, Eliahu N, Rosenthal D, Goloubinoff P. 2001. Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J. Biol. Chem. 276: 39586-39591.
    Pubmed CrossRef
  11. Jehlička J, Oren A, Vítek P. 2012. Use of Raman spectroscopy for identification of compatible solutes in halophilic bacteria. Extremophiles 16: 507-514.
    Pubmed CrossRef
  12. Slama I , Abdelly C , Bouchereau A, Flowers T , Savouré A. 2015. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. 115: 433-447.
    Pubmed PMC CrossRef
  13. Shivanand P, Mugeraya G. 2011. Halophilic bacteria and their compatible solutes-osmoregulation and potential applications. Curr. Sci. 100: 1516-1521.
  14. Xu S, Zhou J, Liu L, Chen J. 2010. Proline enhances Torulopsis glabrata growth during hyperosmotic stress. Biotechnol. Bioproc. E. 15: 285-292.
    CrossRef
  15. Tian X, Wang Y, Chu J, Zhuang Y, Zhang S. 2016. Enhanced l-lactic acid production in Lactobacillus paracasei by exogenous proline addition based on comparative metabolite profiling analysis. Appl. Microbiol. Biot. 100: 2301-2310.
    Pubmed CrossRef
  16. Morita Y, Nakamori S, Takagi H. 2002. Effect of proline and arginine metabolism on freezing stress of Saccharomyces cerevisiae. J. Biosci. Bioeng. 94: 390-394.
    CrossRef
  17. Sheehan VM, Sleator RD, Fitzgerald GF, Hill C. 2006. Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl. Environ. Microb. 72: 2170-2177.
    Pubmed PMC CrossRef
  18. Wu CD, Zhang J , Wang M, Du GC, Chen J. 2 012. Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J. Ind. Microbiol. Biot. 39: 1031-1039.
  19. Zhang J , Wu CD, Du GC, Chen J. 2 012. E nhanced a cid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol. Bioproc. E. 17: 283-289.
  20. Wu R, Song X, Liu Q, Ma D, Xu F, Wang Q, Tang X, Wu J. 2016. Gene expression of Lactobacillus plantarum FS5-5 in response to salt stress. Ann. Microbiol. 66: 1181-1188.
    CrossRef
  21. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25: 402-408.
    Pubmed CrossRef
  22. Brill J, Hoffmann T, Bleisteiner M, Bremer E. 2011. Osmotically controlled synthesis of the compatible solute proline is critical for cellular defense of Bacillus subtilis against high osmolarity. J. Bacteriol. 193: 5335-5346.
    Pubmed PMC CrossRef
  23. Tymczyszyn EE, Gómez A, Disalvo EA. 2005. Influence of the growth at high osmolality on the lipid composition, water permeability and osmotic response of Lactobacillus bulgaricus. Arch. Biochem. Biophys. 443: 66-73.
    Pubmed CrossRef
  24. Guillot A, Obis D, Mistou MY. 2000. Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int. J. Food Microbiol. 55: 47-51.
    CrossRef
  25. Mykytczuk N, Trevors J , Leduc L , Ferroni G . 2007. Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog. Biophys. Mol. Bio. 95: 60-82.
    Pubmed CrossRef
  26. Kempf B, Bremer E. 1998. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170: 319-330.
    Pubmed CrossRef
  27. Joghee NN, Jayaraman G. 2014. Metabolomic characterization of halophilic bacterial isolates reveals strains synthesizing rare diaminoacids under salt stress. Biochimie 102: 102-111.
    Pubmed CrossRef
  28. He Z, Zhou A, Baidoo E, He Q, Joachimiak MP, Benke P, et al. 2010. Global transcriptional, physiological, and metabolite analyses of the responses of Desulfovibrio vulgaris Hildenborough to salt adaptation. Appl. Environ. Microb. 76: 1574-1586.
    Pubmed PMC CrossRef
  29. Vrancken G, Rimaux T, Wouters D, Leroy F, De Vuyst L. 2009. The arginine deiminase pathway of Lactobacillus fermentum IMDO 130101 responds to growth under stress conditions of both temperature and salt. Food Microbiol. 26: 720-727.
    Pubmed CrossRef
  30. Kusvuran S, Dasgan HY, Abak K. 2013. Citrulline is an important biochemical indicator in tolerance to saline and drought stresses in melon. Scientific World J. 2013: 253414.
    Pubmed PMC CrossRef
  31. Held C, Sadowski G. 2016. Compatible solutes: thermodynamic properties relevant for effective protection against osmotic stress. Fluid. Phase. Equilibr. 407: 224-235.
    CrossRef
  32. Triadó X, Vila X, Galinski EA. 2011. Osmoadaptative accumulation of Nε-acetyl-β-lysine in green sulfur bacteria and Bacillus cereus CECT 148T. FEMS Microbiol. Lett. 318:159-167.
    Pubmed CrossRef
  33. Kets E, Galinski EA, De Wit M, De Bont J, Heipieper HJ. 1996. Mannitol, a novel bacterial compatible solute in Pseudomonas putida S12. J. Bacteriol. 178: 6665-6670.
    Pubmed PMC CrossRef
  34. Sand M, Rodrigues M, González JM, Crécy-Lagard V, Santos H , Müller V, et al. 2015. Mannitol-1-phosphate dehydrogenases/phosphatases: a family of novel bifunctional enzymes for bacterial adaptation to osmotic stress. Environ. Microbiol. 17: 711-719.
    Pubmed CrossRef
  35. Denslow SA, Walls AA, Daub ME. 2005. Regulation of biosynthetic genes and antioxidant properties of vitamin B6 vitamers during plant defense responses. Physiol. Mol. Plant P. 66: 244-255.
    CrossRef
  36. Danon A, Miersch O, Felix G, Camp RG, Apel K. 2 005. Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J. 41: 68-80.
    Pubmed CrossRef
  37. Pu X, An M, Han L, Zhang X. 2015. Protective effect of spermidine on salt stress induced oxidative damage in two Kentucky bluegrass (Poa pratensis L.) cultivars. Ecotox. Environ. Safe 117: 96-106.
    Pubmed CrossRef
  38. Zhang G , Xu SC, Hu QZ, Mao W H, Gong YM. 2014. Putrescine plays a positive role in salt-tolerance mechanisms by reducing oxidative damage in roots of vegetable soybean. J. Integr. Agr. 13: 349-357.
    CrossRef
  39. Hirakawa H, Hayashi M, Yamaguchi A, Nishino K. 2010. Indole enhances acid resistance in Escherichia coli. Microb. Pathogenesi. 49: 90-94.
    Pubmed CrossRef
  40. Jayakannan M, Bose J, Babourina O , Rengel Z, Shabala S. 2015. Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regul. 76: 25-40.
    CrossRef
  41. Xie Z , Duan L, Tian X, Wang B, Eneji A E, Li Z. 2 008. Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J. Plant Physiol. 165: 375-384.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(9): 1681-1691

Published online September 28, 2017 https://doi.org/10.4014/jmb.1702.02060

Copyright © The Korean Society for Microbiology and Biotechnology.

Effect of Exogenous Proline on Metabolic Response of Tetragenococcus halophilus under Salt Stress

Guiqiang He 1, 2, Chongde Wu 1, 2*, Jun Hunag 1, 2 and Rongqing Zhou 1, 2

1College of Light Industry, Textile & Food Engineering, Sichuan University, Chengdu 610065, P.R. China, 1Key Laboratory of Leather Chemistry and Engineering, Ministry of Education, Sichuan University, Chengdu 610065, P.R. China

Received: February 23, 2017; Accepted: June 23, 2017

Abstract

This study investigated the effect of proline addition on the salt tolerance of Tetragenococcus
halophilus. Salt stress led to the accumulation of intracellular proline in T. halophilus. When
0.5 g/l proline was added to hyperhaline medium, the biomass increased 34.6% (12% NaCl)
and 27.7% (18% NaCl) compared with the control (without proline addition), respectively. A
metabolomic approach was employed to reveal the cellular metabolic responses and
protective mechanisms of proline upon salt stress. The results showed that both the cellular
membrane fatty acid composition and metabolite profiling responded by increasing
unsaturated and cyclopropane fatty acid proportions, as well as accumulating some specific
intracellular metabolites (environmental stress protector). Higher contents of intermediates
involved in glycolysis, the tricarboxylic acid cycle, and the pentose phosphate pathway were
observed in the cells supplemented with proline. In addition, addition of proline resulted in
increased concentrations of many organic osmolytes, including glutamate, alanine, citrulline,
N-acetyl-tryptophan, and mannitol, which may be beneficial for osmotic homeostasis. Taken
together, results in this study suggested that proline plays a protective role in improving the
salt tolerance of T. halophilus by regulating the related metabolic pathways.

Keywords: Tetragenococcus halophilus, salt stress, metabolic response, proline, metabolomic

References

  1. Tanasupawat S, Thongsanit J, Okada S, Komagata K. 2002. Lactic acid bacteria isolated from soy sauce mash in Thailand. J. Gen. Appl. Microbiol. 48: 201-209.
    Pubmed CrossRef
  2. Hanagata H, Shida O, Takagi H. 2003. Taxonomic homogeneity of a salt-tolerant lactic acid bacteria isolated from shoyu mash. J. Gen. Appl. Microbiol. 49: 95-100.
    Pubmed CrossRef
  3. Wu C D, Liu C L, He GQ, Huang J, Zhou RQ. 2013. Characterization of a multiple-stress tolerance Tetragenococcus halophilus and application as starter culture in Chinese Horsebean-Chili-Paste manufacture for quality improvement. Food Sci. Technol. Res. 19: 855-864.
    CrossRef
  4. Cui RY, Zheng J, Wu CD, Zhou RQ. 2014. Effect of different halophilic microbial fermentation patterns on the volatile compound profiles and sensory properties of soy sauce moromi. Eur. Food Res. Technol. 239: 321-331.
    CrossRef
  5. Roling W, Van Verseveld H. 1996. Characterization of Tetragenococcus halophila populations in indonesian soy mash (Kecap) fermentation. Appl. Environ. Microb. 62: 1203-1207.
    Pubmed KoreaMed
  6. Udomsil N, Rodtong S, Choi YJ, Hua Y, Yongsawatdigul J. 2011. Use of Tetragenococcus halophilus as a starter culture for flavor improvement in fish sauce fermentation. J. Agr. Food Chem. 59: 8401-8408.
    Pubmed CrossRef
  7. Hahne H, Mäder U, Otto A, Bonn F, Steil L, Bremer E, et al. 2010. A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J. Bacteriol. 192: 870-882.
    Pubmed KoreaMed CrossRef
  8. Kilstrup M, Jacobsen S, Hammer K, Vogensen FK. 1997. Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl. Environ. Microb. 63:1826-1837.
    Pubmed KoreaMed
  9. Beales N. 2004. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Compr. Rev. Food Sci. Food 3: 1-20.
    CrossRef
  10. Diamant S, Eliahu N, Rosenthal D, Goloubinoff P. 2001. Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J. Biol. Chem. 276: 39586-39591.
    Pubmed CrossRef
  11. Jehlička J, Oren A, Vítek P. 2012. Use of Raman spectroscopy for identification of compatible solutes in halophilic bacteria. Extremophiles 16: 507-514.
    Pubmed CrossRef
  12. Slama I , Abdelly C , Bouchereau A, Flowers T , Savouré A. 2015. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. 115: 433-447.
    Pubmed KoreaMed CrossRef
  13. Shivanand P, Mugeraya G. 2011. Halophilic bacteria and their compatible solutes-osmoregulation and potential applications. Curr. Sci. 100: 1516-1521.
  14. Xu S, Zhou J, Liu L, Chen J. 2010. Proline enhances Torulopsis glabrata growth during hyperosmotic stress. Biotechnol. Bioproc. E. 15: 285-292.
    CrossRef
  15. Tian X, Wang Y, Chu J, Zhuang Y, Zhang S. 2016. Enhanced l-lactic acid production in Lactobacillus paracasei by exogenous proline addition based on comparative metabolite profiling analysis. Appl. Microbiol. Biot. 100: 2301-2310.
    Pubmed CrossRef
  16. Morita Y, Nakamori S, Takagi H. 2002. Effect of proline and arginine metabolism on freezing stress of Saccharomyces cerevisiae. J. Biosci. Bioeng. 94: 390-394.
    CrossRef
  17. Sheehan VM, Sleator RD, Fitzgerald GF, Hill C. 2006. Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl. Environ. Microb. 72: 2170-2177.
    Pubmed KoreaMed CrossRef
  18. Wu CD, Zhang J , Wang M, Du GC, Chen J. 2 012. Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J. Ind. Microbiol. Biot. 39: 1031-1039.
  19. Zhang J , Wu CD, Du GC, Chen J. 2 012. E nhanced a cid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol. Bioproc. E. 17: 283-289.
  20. Wu R, Song X, Liu Q, Ma D, Xu F, Wang Q, Tang X, Wu J. 2016. Gene expression of Lactobacillus plantarum FS5-5 in response to salt stress. Ann. Microbiol. 66: 1181-1188.
    CrossRef
  21. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25: 402-408.
    Pubmed CrossRef
  22. Brill J, Hoffmann T, Bleisteiner M, Bremer E. 2011. Osmotically controlled synthesis of the compatible solute proline is critical for cellular defense of Bacillus subtilis against high osmolarity. J. Bacteriol. 193: 5335-5346.
    Pubmed KoreaMed CrossRef
  23. Tymczyszyn EE, Gómez A, Disalvo EA. 2005. Influence of the growth at high osmolality on the lipid composition, water permeability and osmotic response of Lactobacillus bulgaricus. Arch. Biochem. Biophys. 443: 66-73.
    Pubmed CrossRef
  24. Guillot A, Obis D, Mistou MY. 2000. Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int. J. Food Microbiol. 55: 47-51.
    CrossRef
  25. Mykytczuk N, Trevors J , Leduc L , Ferroni G . 2007. Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog. Biophys. Mol. Bio. 95: 60-82.
    Pubmed CrossRef
  26. Kempf B, Bremer E. 1998. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170: 319-330.
    Pubmed CrossRef
  27. Joghee NN, Jayaraman G. 2014. Metabolomic characterization of halophilic bacterial isolates reveals strains synthesizing rare diaminoacids under salt stress. Biochimie 102: 102-111.
    Pubmed CrossRef
  28. He Z, Zhou A, Baidoo E, He Q, Joachimiak MP, Benke P, et al. 2010. Global transcriptional, physiological, and metabolite analyses of the responses of Desulfovibrio vulgaris Hildenborough to salt adaptation. Appl. Environ. Microb. 76: 1574-1586.
    Pubmed KoreaMed CrossRef
  29. Vrancken G, Rimaux T, Wouters D, Leroy F, De Vuyst L. 2009. The arginine deiminase pathway of Lactobacillus fermentum IMDO 130101 responds to growth under stress conditions of both temperature and salt. Food Microbiol. 26: 720-727.
    Pubmed CrossRef
  30. Kusvuran S, Dasgan HY, Abak K. 2013. Citrulline is an important biochemical indicator in tolerance to saline and drought stresses in melon. Scientific World J. 2013: 253414.
    Pubmed KoreaMed CrossRef
  31. Held C, Sadowski G. 2016. Compatible solutes: thermodynamic properties relevant for effective protection against osmotic stress. Fluid. Phase. Equilibr. 407: 224-235.
    CrossRef
  32. Triadó X, Vila X, Galinski EA. 2011. Osmoadaptative accumulation of Nε-acetyl-β-lysine in green sulfur bacteria and Bacillus cereus CECT 148T. FEMS Microbiol. Lett. 318:159-167.
    Pubmed CrossRef
  33. Kets E, Galinski EA, De Wit M, De Bont J, Heipieper HJ. 1996. Mannitol, a novel bacterial compatible solute in Pseudomonas putida S12. J. Bacteriol. 178: 6665-6670.
    Pubmed KoreaMed CrossRef
  34. Sand M, Rodrigues M, González JM, Crécy-Lagard V, Santos H , Müller V, et al. 2015. Mannitol-1-phosphate dehydrogenases/phosphatases: a family of novel bifunctional enzymes for bacterial adaptation to osmotic stress. Environ. Microbiol. 17: 711-719.
    Pubmed CrossRef
  35. Denslow SA, Walls AA, Daub ME. 2005. Regulation of biosynthetic genes and antioxidant properties of vitamin B6 vitamers during plant defense responses. Physiol. Mol. Plant P. 66: 244-255.
    CrossRef
  36. Danon A, Miersch O, Felix G, Camp RG, Apel K. 2 005. Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J. 41: 68-80.
    Pubmed CrossRef
  37. Pu X, An M, Han L, Zhang X. 2015. Protective effect of spermidine on salt stress induced oxidative damage in two Kentucky bluegrass (Poa pratensis L.) cultivars. Ecotox. Environ. Safe 117: 96-106.
    Pubmed CrossRef
  38. Zhang G , Xu SC, Hu QZ, Mao W H, Gong YM. 2014. Putrescine plays a positive role in salt-tolerance mechanisms by reducing oxidative damage in roots of vegetable soybean. J. Integr. Agr. 13: 349-357.
    CrossRef
  39. Hirakawa H, Hayashi M, Yamaguchi A, Nishino K. 2010. Indole enhances acid resistance in Escherichia coli. Microb. Pathogenesi. 49: 90-94.
    Pubmed CrossRef
  40. Jayakannan M, Bose J, Babourina O , Rengel Z, Shabala S. 2015. Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regul. 76: 25-40.
    CrossRef
  41. Xie Z , Duan L, Tian X, Wang B, Eneji A E, Li Z. 2 008. Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J. Plant Physiol. 165: 375-384.
    Pubmed CrossRef