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Applied and Environmental Microbiology, January 2006, p. 404-411, Vol. 72, No. 1
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.1.404-411.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Expression of Transcription Activator ComK of Bacillus subtilis in the Heterologous Host Lactococcus lactis Leads to a Genome-Wide Repression Pattern: a Case Study of Horizontal Gene Transfer

Kim A. Susanna, Chris D. den Hengst, Leendert W. Hamoen, and Oscar P. Kuipers^*

Department of Genetics, University of Groningen, NL-9751 NN Haren, The Netherlands

Received 19 July 2005/ Accepted 7 October 2005

Horizontal gene transfer (HGT) is generally considered a possible mechanism by which bacteria acquire new genetic properties. Especially when pathogenicity genes are involved, HGT might have important consequences for humans. In this report we describe a case study of HGT in which a transcriptional activator, ComK of Bacillus subtilis, was introduced into a heterologous host species, Lactococcus lactis. ComK is the central regulator of competence development, activating transcription by binding to a ComK-binding site, a so-called K-box. Interestingly, L. lactis does not contain a comK gene, but it does contain almost 400 putatively functional K-boxes, as well as homologues of a number of competence genes. In this study, the effect of HGT of B. subtilis comK into L. lactis was investigated by determining the effects on the transcription profile using DNA microarray analyses. Production of wild-type ComK was shown to stimulate the transcription of 89 genes and decrease the expression of 114 genes. Notably, potential direct effects (i.e., genes preceded by a K-box) were found mainly among repressed genes, suggesting that ComK functions as a repressor in L. lactis. This is a remarkable difference between L. lactis and B. subtilis, in which ComK almost exclusively activates transcription. Additional DNA microarray analyses with a transcription activation-deficient but DNA-binding ComK variant, ComKC25, demonstrated that there were similar effects on gene regulation with this variant and with wild-type ComK, confirming that the direct effects of ComK result from interference with normal transcription through binding to available K-boxes. This study demonstrates that horizontal gene transfer can have dramatic effects that are very different than those that are expected on basis of the original functionality of a gene.

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* Corresponding author. Mailing address: Department of Genetics, University of Groningen, NL-9751 NN Haren, The Netherlands. Phone: 31(0)50 363 2093. Fax: 31(0)50 363 2348. E-mail: O.P.Kuipers{at}rug.nl

Present address: Department of Pharmaceutical Biosciences, School of Pharmacy, University of Oslo, PO Box 1068 Blindern, 0316 Oslo, Norway.

Present address: Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford OX1 3RE, United Kingdom.

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Applied and Environmental Microbiology, January 2006, p. 404-411, Vol. 72, No. 1
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.1.404-411.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

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