Article

Free Access

Proteomic Characterization of Enterohemorrhagic Escherichia coli O157:H7 in the Oxidation-Induced Viable but Non-Culturable State

Corresponding Author

Hiroshi Asakura

Division of Biomedical Food Research, National Institute of Health Sciences, Setagaya-ku, Tokyo, 158-8501 Japan

Address correspondence to Dr. Hiroshi Asakura, Division of Biomedical Food Research, National Institute of Health Sciences, Kamiyoga 1-18-1, Setagaya-ku, Tokyo 158-8501, Japan. Fax: +81-3-3700-9246. E-mail: [email protected]Search for more papers by this author

Nantika Panutdaporn,

Nantika Panutdaporn

Laboratory of Food Microbiology and Immunology, Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555 Japan

Search for more papers by this author

Keiko Kawamoto,

Keiko Kawamoto

Laboratory of Food Microbiology and Immunology, Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555 Japan

Search for more papers by this author

Shizunobu Igimi,

Shizunobu Igimi

Division of Biomedical Food Research, National Institute of Health Sciences, Setagaya-ku, Tokyo, 158-8501 Japan

Search for more papers by this author

Shigeki Yamamoto,

Shigeki Yamamoto

Division of Biomedical Food Research, National Institute of Health Sciences, Setagaya-ku, Tokyo, 158-8501 Japan

Search for more papers by this author

Sou-ichi Makino,

Sou-ichi Makino

Laboratory of Food Microbiology and Immunology, Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555 Japan

Search for more papers by this author

Hiroshi Asakura,

Corresponding Author

Hiroshi Asakura

Division of Biomedical Food Research, National Institute of Health Sciences, Setagaya-ku, Tokyo, 158-8501 Japan

Nantika Panutdaporn,

Nantika Panutdaporn

Laboratory of Food Microbiology and Immunology, Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555 Japan

Search for more papers by this author

Keiko Kawamoto,

Keiko Kawamoto

Laboratory of Food Microbiology and Immunology, Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555 Japan

Search for more papers by this author

Shizunobu Igimi,

Shizunobu Igimi

Division of Biomedical Food Research, National Institute of Health Sciences, Setagaya-ku, Tokyo, 158-8501 Japan

Search for more papers by this author

Shigeki Yamamoto,

Shigeki Yamamoto

Division of Biomedical Food Research, National Institute of Health Sciences, Setagaya-ku, Tokyo, 158-8501 Japan

Search for more papers by this author

Sou-ichi Makino,

Sou-ichi Makino

Laboratory of Food Microbiology and Immunology, Research Center for Animal Hygiene and Food Safety, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555 Japan

Search for more papers by this author

First published: 14 November 2013

https://doi.org/10.1111/j.1348-0421.2007.tb03969.x

Citations: 41

Share a link

Email
Wechat
Bluesky

Abstract

Enterohemorrhagic Escherichia coli (EHEC) O157 strain F2, a food isolate of an outbreak, is resistant to oxidative stress, but has increased stress-sensitivity after passage through mice. The stress-sensitive variant of F2 (designated MP37) has decreased culturability, but retains membrane integrity under stress conditions, indicating that the cells enter a viable but non-culturable (VBNC) state. Proteomic analyses revealed that MP37 in the VBNC state had decreased levels of some oxidation-responsive factors (AhpCF, AceF), but it markedly increased levels of outer membrane protein W (OmpW). Because F2 expressed higher levels of some ribosome-associated proteins (RaiA, S6, Bcp) than MP37, the effect of animal passage on the induction of the VBNC state in the EHEC O157 cells might be due to ribosomal activity.

Abbreviations

AceF: dihydrolipoyllysine-residue acetyltransferase
Ahp: alkyl hydroperoxide reductase
Bcp: bacterioferritin comigratory protein
EHEC: enterohemorrhagic Escherichia coli
EF-TU: elongation factor
LpdA: lipoamide dehydrogenase
OmpW: outer membrane protein W
OxyR: oxidative stress regulator
PBS: phosphate buffered saline
RpoS: RNA polymerase sigma subunit
SurA: peptidyl-prolyl cis-transisomerase
TSA: tryptic soy agar
TSA-SP: TSA amended with 0.1% sodium pyruvate
2-DE: two-dimensional gel electrophoresis
VBNC: viable but non-culturable.

References

1Agafonov, D.E., Kolb, V.A., and Spirin, A.S. 2001. A novel stress-response protein that binds at the ribosomal subunit interface and arrests translation. Cold Spring Harb. Symp. Quant. Biol. 66: 509–514.
10.1101/sqb.2001.66.509
CAS PubMed Web of Science® Google Scholar
2Asakura, H., Makino, S., Takagi, T., Kuri, A., Kurazono, T., Watarai, M., and Shirahata, T. 2002. Passage in mice causes a change in the ability of Salmonella enterica serovar Oranienburg to survive NaCl osmotic stress: resuscitation from the viable but non-culturable state. FEMS Microbiol. Lett. 212: 87–93.
10.1111/j.1574-6968.2002.tb11249.x
CAS PubMed Web of Science® Google Scholar
3Asakura, H., Igimi, S., Kawamoto, K., Yamamoto, S., and Makino, S. 2005. Role of in vivo passage on the environmental adaptation of enterohemorrhagic Escherichia coli O157:H7: cross-induction of the viable but nonculturable state by osmotic and oxidative stresses. FEMS Microbiol. Lett. 253: 243–249.
10.1016/j.femsle.2005.09.039
CAS PubMed Web of Science® Google Scholar
4Chaveerach, P., Huurne, A.A., Lipman, L.J., and Van Knapen, F. 2003. Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl. Environ. Microbiol. 69: 711–714.
10.1128/AEM.69.1.711-714.2003
CAS PubMed Web of Science® Google Scholar
5Das, H.K., and Goldstein, A. 1968. Limited capacity for protein synthesis at zero degrees centigrade in Escherichia coli. J. Mol. Biol. 31: 209–226.
10.1016/0022-2836(68)90440-3
CAS PubMed Web of Science® Google Scholar
6Gupte, A.R., De Rezende, C.L., and Joseph, S.W. 2003. Induction and resuscitation of viable but nonculturable Salmonella enterica serovar typhimurium DT104. Appl. Environ. Microbiol. 69: 6669–6675.
10.1128/AEM.69.11.6669-6675.2003
CAS PubMed Web of Science® Google Scholar
7Heim, S., Lleo, M.M., Bonato, B., Guzman, C.A., and Canepari, P. 2002. The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J. Bacteriol. 184: 6739–6745.
10.1128/JB.184.23.6739-6745.2002
CAS PubMed Web of Science® Google Scholar
8Hoffmann, F., Weber, J., and Rinas, U. 2002. Metabolic adaptation of Escherichia coli during temperature-induced recombinant protein production: 1. Readjustment of metabolic enzyme synthesis. Biotechnol. Bioeng. 80: 313–319.
10.1002/bit.10379
CAS PubMed Web of Science® Google Scholar
9Kolling, G.L., and Matthews, K.R. 2001. Examination of recovery in vitro and in vivo of nonculturable Escherichia coli O157:H7. Appl. Environ. Microbiol. 67: 3928–3933.
10.1128/AEM.67.9.3928-3933.2001
CAS PubMed Web of Science® Google Scholar
10Lund, P.A. 2001. Microbial molecular chaperones. Adv. Microb. Physiol. 44: 93–140.
10.1016/S0065-2911(01)44012-4
CAS PubMed Web of Science® Google Scholar
11Makino, S., Kii, T., Asakura, H., Shirahata, T., Ikeda, T., and Takeshi, K. 2000. Does enterohemorrhagic Escherichia coli O157:H7 enter the viable but nonculturable state in salted salmon roe? Appl. Environ. Microbiol. 66: 5536–5539.
10.1128/AEM.66.12.5536-5539.2000
CAS PubMed Web of Science® Google Scholar
12Mizunoe, Y., Wai, S.N., Takade, A., and Yoshida, S. 1999. Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli O157 cells by using H₂O₂-degrading compounds. Arch. Microbiol. 172: 63–67.
10.1007/s002030050741
CAS PubMed Web of Science® Google Scholar
13Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67: 593–656.
10.1128/MMBR.67.4.593-656.2003
CAS PubMed Web of Science® Google Scholar
14Oliver, J.D. 2005. The viable but nonculturable state in bacteria. J. Microbiol. 43: 93–100.
PubMed Web of Science® Google Scholar
15Pilsl, H., Smajs, D., and Braun, V. 1999. Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. J. Bacteriol. 181: 3578–3581.
CAS PubMed Web of Science® Google Scholar
16Rocha, E.P., Matic, I., and Taddei, F. 2002. Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions? Nucleic Acids Res. 30: 1886–1894.
10.1093/nar/30.9.1886
CAS PubMed Web of Science® Google Scholar
17Rozen, Y., and Belkin, S. 2001. Survival of enteric bacteria in seawater. FEMS Microbiol. Rev. 25: 513–529.
10.1111/j.1574-6976.2001.tb00589.x
CAS PubMed Web of Science® Google Scholar
18Sainz, T., Perez, J., Villaseca, J., Hernandez, U., Eslava, C., Mendoza, G., and Wacher, C. 2005. Survival to different acid challenges and outer membrane protein profiles of pathogenic Escherichia coli strains isolated from pozol, a Mexican typical maize fermented food. Int. J. Food Microbiol. 105: 357–367.
10.1016/j.ijfoodmicro.2005.04.017
CAS PubMed Web of Science® Google Scholar
19Storz, G., and Zheng, M. 2000. Oxidative stress, p. 47–59. In G. Storz, and R. Hengge-Aronis (eds), Bacterial stress responses, ASM Press, Washington, D.C.
Google Scholar
20Wu, L., Lin, X., Wang, F., Ye, D., Xiao, X., Wang, S., and Peng, X. 2006. OmpW and OmpV are required for NaCl regulation in Photobacterium damsela. J. Proteome Res. 5: 2250–2257.
10.1021/pr060046c
CAS PubMed Web of Science® Google Scholar
21Xu, C., Wang, S., Ren, H., Lin, X., Wu, L., and Peng, X. 2005. Proteomic analysis on the expression of outer membrane proteins of Vibrio alginolyticus at different sodium concentrations. Proteomics 5: 3142–3152.
10.1002/pmic.200401128
CAS PubMed Web of Science® Google Scholar
22Yaron, S., and Matthews, K.R. 2002. A reverse transcriptase-polymerase chain reaction assay for detection of viable Escherichia coli O157:H7: investigation of specific target genes. J. Appl. Microbiol. 92: 633–640.
10.1046/j.1365-2672.2002.01563.x
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume51, Issue9

September 2007

Pages 875-881

Proteomic Characterization of Enterohemorrhagic Escherichia coli O157:H7 in the Oxidation-Induced Viable but Non-Culturable State

Abstract

Abbreviations

References

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Proteomic Characterization of Enterohemorrhagic Escherichia coli O157:H7 in the Oxidation-Induced Viable but Non-Culturable State

Abstract

Abbreviations

References

Citing Literature

References

Related

Information