Current Microbiology

, Volume 75, Issue 1, pp 20–26 | Cite as

Proteomic Analysis of Vibrio parahaemolyticus Under Cold Stress

  • Jing Tang
  • Juntao Jia
  • Ying Chen
  • Xiaohua Huang
  • Xiaoliang Zhang
  • Liqing Zhao
  • Wei Hu
  • Changjun Wang
  • Chao Lin
  • Zhenxing Wu
Article

Abstract

Vibrio parahaemolyticus is a kind of food-borne pathogenic bacterium, which can seriously infect food, especially seafood causing gastroenteritis and other disease. We studied the global proteome responses of V. parahaemolyticus under cold stress by nano-liquid chromatography-tandem mass spectrometry to improve the present understanding of V. parahaemolyticus proteomics events under cold stress. A total of 1151 proteins were identified and 101 proteins were differentially expressed, of which 69 were significantly up-regulated and 32 were downregulated. Functional categorization of these proteins revealed distinct differences between cold-stressed and control cells. These proteins were grouped into 21 functional categories by the clusters of orthologous groups (COG) analysis. The most of up-regulated proteins were functionally categorized as nucleotide transport and metabolism, transcription, function unknown, and defense mechanisms. These up-regulated proteins play an important role under cold stress.

Notes

Acknowledgements

We thank Dr. Mingwei Liu (Beijing Proteome Research Center) for sample preparation and Mass Spectrometry analysis. This work was supported by the Chinese State High-Tech Development Plan (2012AA101605), the Science Foundation of General Administration of Quality Supervision, Inspection, and Quarantine of the People’s Republic of China (2012IK305, 2013IK175, and 2016IK198).

Supplementary material

284_2017_1345_MOESM1_ESM.xlsx (115 kb)
Supplementary material 1 (XLSX 115 kb)

References

  1. 1.
    Feldhusen F (2000) The role of seafood in bacterial foodborne diseases. Microbes Infect 2:1651–1660CrossRefPubMedGoogle Scholar
  2. 2.
    Liston J (1990) Microbial hazards of seafood consumption. Food Technol 44:56–62Google Scholar
  3. 3.
    Su YC, Liu C (2007) Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol 24:549–558CrossRefPubMedGoogle Scholar
  4. 4.
    Chiang ML, Ho WL, Chou CC (2008) Ethanol shock changes the fatty acid profile and survival behavior of Vibrio parahaemolyticus in various stress conditions. Food Microbiol 25:359–365CrossRefPubMedGoogle Scholar
  5. 5.
    Browne N, Dowds BC (2002) Acid stress in the food pathogen Bacillus cereus. J Appl Microbiol 92:404–414CrossRefPubMedGoogle Scholar
  6. 6.
    Lou Y, Yousef AE (1997) Adaptation to sublethal environmental stress protects Listeria monocytogenes against lethal preservation factors. Appl Environ Microbiol 63:1252–1255PubMedPubMedCentralGoogle Scholar
  7. 7.
    Gualerzi CO, Pon CL (1990) Initiation of mRNA translation in prokaryotes. Biochemistry 29:5881–5889CrossRefPubMedGoogle Scholar
  8. 8.
    Phadtare S (2004) Recent developments in bacterial cold-shock response. Curr Issues Mol Biol 6:125–136PubMedGoogle Scholar
  9. 9.
    Phadtare S, Alsina J, Inouye M (1999) Cold-shock response and cold-shock proteins. Curr Opin Microbiol 2:175–180CrossRefPubMedGoogle Scholar
  10. 10.
    Weber MH, Marahiel MA (2003) Bacterial cold shock responses. Sci Prog 86:9–75CrossRefPubMedGoogle Scholar
  11. 11.
    Jia J, Chen Y, Jiang Y, Tang J, Yang L, Liang C, Jia Z, Zhao L (2014) Visualized analysis of cellular fatty acid profiles of Vibrio parahaemolyticus strains under cold stress. FEMS Microbiol Lett 357:92–98CrossRefPubMedGoogle Scholar
  12. 12.
    Xuan G, Jia J, Chen Y, Wang J, Tang J, Jiang Y, Xu B, Liang C, Li M (2015) Strain-level visualized analysis of cold-stressed Vibrio parahaemolyticus based on MALDI–TOF mass fingerprinting. Microb Pathog 88:16–21CrossRefPubMedGoogle Scholar
  13. 13.
    Lilley KS, Razzaq A, Dupree P (2002) Two-dimensional gel electrophoresis: recent advances in sample preparation, detection and quantitation. Curr Opin Chem Biol 6:46–50CrossRefPubMedGoogle Scholar
  14. 14.
    Durack J, Ross T, Bowman JP (2013) Characterisation of the transcriptomes of genetically diverse Listeria monocytogenes exposed to hyperosmotic and low temperature conditions reveal global stress-adaptation mechanisms. PLoS ONE 8:e73603CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    López-Ferrer D, Martínez-Bartolomé S, Villar M, Campillos M, Martín-Maroto F, Vázquez J (2004) Statistical model for large-scale peptide identification in databases from tandem Mass Spectra using SEQUEST. Anal Chem 76:6853–6860CrossRefPubMedGoogle Scholar
  16. 16.
    Zhou L, Zhao SZ, Koh SK, Chen L, Vaz C, Tanavde V, Li XR, Beuerman RW (2012) In-depth analysis of the human tear proteome. J Proteom 75:3877–3885CrossRefGoogle Scholar
  17. 17.
    Griffiths JR, Chicooree N, Connolly Y, Neffling M, Lane CS, Knapman T, Smith DL (2014) Mass spectral enhanced detection of Ubls using SWATH acquisition: MEDUSA—simultaneous quantification of SUMO and ubiquitin-derived isopeptides. J Am Soc Mass Spectrom 25:767–777CrossRefPubMedGoogle Scholar
  18. 18.
    Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, Sevinsky JR, Resing KA, Ahn NG (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteom 4:1487–1502CrossRefGoogle Scholar
  19. 19.
    Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Wu S, Zhu Z, Fu L, Niu B, Li W (2011) WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genom 12:444CrossRefGoogle Scholar
  21. 21.
    Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, Taylor TD, Noguchi H, Mori H, Ogura Y, Ehrlich DS, Itoh K, Takagi T, Sakaki Y, Hayashi T, Hattori M (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14:169–181CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Kim EY, Kim YR, Kim DG, Kong IS (2012) A susceptible protein by proteomic analysis from Vibrio anguillarum under various environmental conditions. Bioprocess Biosyst Eng 35:273–282CrossRefPubMedGoogle Scholar
  23. 23.
    Vorob’eva LI (2004) Stressors, stress reactions and survival of bacteria. Prikl Biokhim Mikrobiol 40:261–269PubMedGoogle Scholar
  24. 24.
    Polissi A, De Laurentis W, Zangrossi S, Briani F, Longhi V, Pesole G, Dehò G (2003) Changes in Escherichia coli transcriptome during acclimatization at low temperature. Res Microbiol 154:573–580CrossRefPubMedGoogle Scholar
  25. 25.
    Wouters JA, Jeynov B, Rombouts FM, de Vos WM, Kuipers OP, Abee T (1999) Analysis of the role of 7 kDa cold-shock proteins of Lactococcus lactis MG1363 in cryoprotection. Microbiology 145:3185–3194CrossRefPubMedGoogle Scholar
  26. 26.
    Charollais J, Dreyfus M, Iost I (2004) CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res 32:2751–2759CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Dersch P, Kneip S, Bremer E (1994) The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol Gen Genet 245:255–259CrossRefPubMedGoogle Scholar
  28. 28.
    Mihoub F, Mistou MY, Guillot A, Leveau JY, Boubetra A, Billaux F (2003) Cold adaptation of Escherichia coli: microbiological and proteomic approaches. Int J Food Microbiol 89:171–184CrossRefPubMedGoogle Scholar
  29. 29.
    Miladi H, Soukri A, Bakhrouf A, Ammar E (2012) Expression of ferritin-like protein in Listeria monocytogenes after cold and freezing stress. Folia Microbiol 57:551–556CrossRefGoogle Scholar
  30. 30.
    Wood RR, Arias CR (2011) Evaluation of global gene expression during cold shock in the human pathogen Vibrio vulnificus. Mar Biotechnol 13:942–954CrossRefPubMedGoogle Scholar
  31. 31.
    Jia J, Chen Y, Jiang Y, Li Z, Zhao L, Zhang J, Tang J, Feng L, Liang C, Xu B, Gu P, Ye X (2015) Proteomic analysis of Vibrio metschnikovii under cold stress using a quadrupole Orbitrap mass spectrometer. Res Microbiol 166:618–625CrossRefPubMedGoogle Scholar
  32. 32.
    Yang L, Zhou D, Liu X, Han H, Zhan L, Guo Z, Zhang L, Qin C, Wong HC, Yang R (2009) Cold-induced gene expression profiles of Vibrio parahaemolyticus: a time-course analysis. FEMS Microbiol Lett 291:50–58CrossRefPubMedGoogle Scholar
  33. 33.
    Jones PG, VanBogelen RA, Neidhardt FC (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169:2092–2095CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Jiang W, Hou Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272:196–202CrossRefPubMedGoogle Scholar
  35. 35.
    Nakashima K, Kanamaru K, Mizuno T, Horikoshi K (1996) A novel member of the cspA family of genes that is induced by cold shock in Escherichia coli. J Bacteriol 178:2994–2997CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Wang N, Yamanaka K, Inouye M (1999) CspI, the ninth member of the CspA family of Escherichia coli, is induced upon cold shock. J Bacteriol 181:1603–1609PubMedPubMedCentralGoogle Scholar
  37. 37.
    Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48:60–93PubMedPubMedCentralGoogle Scholar
  38. 38.
    Sugino A, Peebles CL, Kreuzer KN, Cozzarelli NR (1977) Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc Natl Acad Sci USA 74:4767–4771CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Friedman DI, Olson ER, Georgopoulos C, Tilly K, Herskowitz I, Banuett F (1984) Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda. Microbiol Rev 48:299–325PubMedPubMedCentralGoogle Scholar
  40. 40.
    Thieringer HA, Jones PG, Inouye M (1998) Cold shock and adaptation. BioEssays 20:49–57CrossRefPubMedGoogle Scholar
  41. 41.
    Lelivelt MJ, Kawula TH (1995) Hsc66, an Hsp70 homolog in Escherichia coli, is induced by cold shock but not by heat shock. J Bacteriol 177:4900–4907CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kandror O, DeLeon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Kandror O, Goldberg AL (1997) Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc Natl Acad Sci USA 94:4978–4981CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Toone WM, Rudd KE, Friesen JD (1991) deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J Bacteriol 173:3291–3302CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Dammel CS, Noller HF (1995) Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev 9:626–637CrossRefPubMedGoogle Scholar
  46. 46.
    Chen C, Deutscher MP (2005) Elevation of RNase R in response to multiple stress conditions. J Biol Chem 280:34393–34396CrossRefPubMedGoogle Scholar
  47. 47.
    Qin T, Hu X, Hu J, Wang X (2015) Metabolic engineering of Corynebacterium glutamicum strain ATCC13032 to produce l-methionine. Biotechnol Appl Biochem 62:563–573CrossRefPubMedGoogle Scholar
  48. 48.
    Raïs B, Mazat JP (1995) Control of the metabolic pathway of threonine in E coli. Application of biotechnology. Acta Biotheor 43:143–153CrossRefPubMedGoogle Scholar
  49. 49.
    Tang H, Wang E, Sui X, Man C, Jia R, Lin D, Qu Z, Chen W (2007) The novel alkali tolerance function of tfxG in Sinorhizobium meliloti. Res Microbiol 158:501–505CrossRefPubMedGoogle Scholar
  50. 50.
    Sleator RD, Gahan CG, Hill C (2001) Identification and disruption of the proBA Locus in Listeria monocytogenes: role of proline biosynthesis in salt tolerance and murine infection. Appl Environ Microbiol 67:2571–2577CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Bode M, Longen S, Morgan B, Peleh V, Dick TP, Bihlmaier K, Herrmann JM (2013) Inaccurately assembled cytochrome c oxidase can lead to oxidative stress-induced growth arrest. Antioxid Redox Signal 18:1597–1612CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Usuda Y, Nishio Y, Iwatani S, Van Dien SJ, Imaizumi A, Shimbo K, Kageyama N, Iwahata D, Miyano H, Matsui K (2010) Dynamic modeling of Escherichia coli metabolic and regulatory systems for amino-acid production. J Biotechnol 147:17–30CrossRefPubMedGoogle Scholar
  53. 53.
    Li H, Park JT (1999) The periplasmic murein peptide-binding protein MppA is a negative regulator of multiple antibiotic resistance in Escherichia coli. J Bacteriol 181:4842–4847PubMedPubMedCentralGoogle Scholar
  54. 54.
    Parada C, Orruño M, Kaberdin V, Bravo Z, Barcina I, Arana I (2016) Changes in the Vibrio harveyi cell envelope subproteome during permanence in cold seawater. Microb Ecol 72:549–558CrossRefPubMedGoogle Scholar
  55. 55.
    Jia J, Li Z, Cao J, Jiang Y, Liang C, Liu M (2013) Proteomic analysis of protein expression in the induction of the viable but nonculturable state of Vibrio harveyi SF1. Curr Microbiol 67:442–447CrossRefPubMedGoogle Scholar
  56. 56.
    Chiancone E, Ceci P (2010) The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding. Biochim Biophys Acta 1800:798–805CrossRefPubMedGoogle Scholar
  57. 57.
    Yu F, Inouye S, Inouye M (1986) Lipoprotein-28, a cytoplasmic membrane lipoprotein from Escherichia coli. Cloning, DNA sequence, and expression of its gene. J Biol Chem 261:2284–2288PubMedGoogle Scholar
  58. 58.
    Urmersbach S, Aho T, Alter T, Hassan SS, Autio R, Huehn S (2015) Changes in global gene expression of Vibrio parahaemolyticus induced by cold- and heat-stress. BMC Microbiol 15:229CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Rogers S, Girolami M, Kolch W, Waters KM, Liu T, Thrall B, Wiley HS (2008) Investigating the correspondence between transcriptomic and proteomic expression profiles using coupled cluster models. Bioinformatics 24:2894–2900CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Jing Tang
    • 1
  • Juntao Jia
    • 1
  • Ying Chen
    • 2
  • Xiaohua Huang
    • 1
  • Xiaoliang Zhang
    • 1
  • Liqing Zhao
    • 1
  • Wei Hu
    • 1
  • Changjun Wang
    • 1
  • Chao Lin
    • 1
  • Zhenxing Wu
    • 1
  1. 1.Shandong Entry-Exit Inspection and Quarantine BureauQingdaoPeople’s Republic of China
  2. 2.Chinese Academy of Inspection and QuarantineBeijingChina

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