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J. Biol. Chem., Vol. 279, Issue 33, 34183-34190, August 13, 2004

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ppGpp-dependent Stationary Phase Induction of Genes on Salmonella Pathogenicity Island 1^*

Miryoung Song, Hyun-Ju Kim, Eun Young Kim, Minsang Shin, Hyun Chul Lee, Yeongjin Hong, Joon Haeng Rhee, Hyunjin Yoon¶, Sangryeol Ryu¶, Sangyong Lim¶, and Hyon E. Choy||

From the Genome Research Center for Enteropathogenic Bacteria and Research Institute of Vibrio Infection and the Department of Microbiology, Chonnam National University Medical College, Kwangju 501-746, South Korea and the ^¶Department of Food Science and Technology, School of Agricultural Biotechnology, Center for Agricultural Biomaterials, Seoul National University, Seoul, 151-742, South Korea

We have examined expression of the genes on Salmonella pathogenicity island 1 (SPI1) during growth under the physiologically well defined standard growth condition of Luria-Bertani medium with aeration. We found that the central regulator hilA and the genes under its control are expressed at the onset of stationary phase. Interestingly, the two-component regulatory genes hilC/hilD, sirA/barA, and ompR, which are known to modulate expression from the hilA promoter (hilAp) under so-called "inducing conditions" (Luria-Bertani medium containing 0.3 M NaCl without aeration), acted under standard conditions at the stationary phase induction level. The induction of hilAp depended not on RpoS, the stationary phase sigma factor, but on the stringent signal molecule ppGpp. In the ppGpp null mutant background, hilAp showed absolutely no activity. The stationary phase induction of hilAp required spoT but not relA. Consistent with this requirement, hilAp was also induced by carbon source deprivation, which is known to transiently elevate ppGpp mediated by spoT function. The observation that amino acid starvation elicited by the addition of serine hydroxamate did not induce hilAp in a RelA⁺ SpoT⁺ strain suggested that, in addition to ppGpp, some other alteration accompanying entry into the stationary phase might be necessary for induction. It is speculated that during the course of infection Salmonella encounters various stressful environments that are sensed and translated to the intracellular signal, ppGpp, which allows expression of Salmonella virulence genes, including SPI1 genes.

Received for publication, December 10, 2003 , and in revised form, April 30, 2004.

^* This work was supported by the Ministry of Health and Welfare, Republic of Korea Health 21 Research and Development Grant 01-PJ10-PG6-01GM02-002. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed. Tel.: 82-62-220-4137; Fax: 82-62-228-7294; E-mail: hyonchoy{at}chonnam.ac.kr.

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