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Originally published In Press as doi:10.1074/jbc.M007687200 on November 27, 2000

J. Biol. Chem., Vol. 276, Issue 8, 5700-5706, February 23, 2001
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An Insertion Sequence Prepares Pseudomonas putida S12 for Severe Solvent Stress*

Jan WeryDagger §, Budi Hidayat, Jasper KieboomDagger , and Jan A. M. de BontDagger ||

From the Dagger  Division of Industrial Microbiology, Department of Agrotechnology and Food Sciences, Wageningen University, P. O. Box 8129, 6700 EV Wageningen, The Netherlands

The novel insertion sequence ISS12 plays a key role in the tolerance of Pseudomonas putida S12 to sudden toluene stress. Under normal culturing conditions the P. putida S12 genome contained seven copies of ISS12. However, a P. putida S12 population growing to high cell density after sudden addition of a separate phase of toluene carried eight copies. The survival frequency of cells in this variant P. putida S12 population was 1000 times higher than in "normal" P. putida S12 populations. Analysis of the nucleotide sequence flanking the extra ISS12 insertion revealed integration into the srpS gene. srpS forms a gene cluster with srpR and both are putative regulators of the solvent resistance pump SrpABC. SrpABC makes a major contribution to solvent tolerance in P. putida S12 and is induced by toluene. The basal level of srp promoter activity in the P. putida S12 variant was seven times higher than in wild-type P. putida S12. Introduction of the intact srpRS gene cluster in the variant resulted in a dramatic decrease of survival frequency after a toluene shock. These findings strongly suggest that interruption of srpS by ISS12 up-regulates expression of the solvent pump, enabling the bacterium to tolerate sudden exposure to lethal concentrations of toxic solvents. We propose that P. putida S12 employs ISS12 as a mutator element to generate diverse mutations to swiftly adapt when confronted with severe adverse conditions.

* Supported by Grant BIO4-CT97-2270 from the European Commission.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AF292393.

Present address: Dept. of Molecular Cell Physiology, Faculty of Biology, Free University, De Boelelaan 1087, NL-1081 HV Amsterdam, The Netherlands.

|| Present address: Friesland Coberco Dairy Foods, Corporate Research, P. O. Box 87, 7400 AB Deventer, The Netherlands.

§ To whom correspondence should be addressed: Present address: Friesland Coberco Dairy Foods, Corporate Research, P. O. Box 87, 7400 AB Deventer, The Netherlands. Tel.: 31-317-484-980; Fax: 31-317-484-978; E-mail j.wery@fcdf.nl.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.


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