JB Accepts, published online ahead of print on 21 March 2008

This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Jakubovics, N. S. Articles by Kolenbrander, P. E. Search for Related Content PubMed PubMed Citation Articles by Jakubovics, N. S. Articles by Kolenbrander, P. E.

 Previous Article  |  Next Article 

J. Bacteriol. doi:10.1128/JB.00088-08
Copyright (c) 2008, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Regulation of gene expression in a mixed-genus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii

Nicholas S. Jakubovics, Steven R. Gill, Stacey E. Iobst, M. M. Vickerman, and Paul E. Kolenbrander^*

National Institute of Dental and Craniofacial Research, National Institutes of Health, Building 30, Room 310, Bethesda, Maryland 20892, Department of Oral Biology, University at Buffalo School of Dentistry, Buffalo, NY, USA, Institute for Genomic Research, 9712 Medical Center Drive, Rockville, MD 20850

^* To whom correspondence should be addressed. Email: pkolenbrander{at}dir.nidcr.nih.gov.

Interactions involving genetically distinct bacteria, for example between oral streptococci and actinomyces, are central to dental plaque development. A DNA microarray identified Streptococcus gordonii genes regulated in response to coaggregation with Actinomyces naeslundii. Expression of 23 genes changed >3-fold in coaggregates, including nine genes involved in arginine biosynthesis and transport. The capacity of S. gordonii to synthesize arginine was assessed using a chemically defined growth medium. In monoculture, streptococcal arginine biosynthesis was inefficient and streptococci could not grow aerobically in low arginine. In dual-species cultures containing coaggregates, however, S. gordonii grew to high cell density in low arginine. Equivalent co-cultures without coaggregates showed no growth until coaggregation was evident (9 h). An argH mutant was unable to grow in low arginine with or without A. naeslundii, indicating that arginine biosynthesis was essential for coaggregation-induced streptococcal growth. Using quantitative RT-PCR, expression of argC, argG and pyrA_b was strongly (10- to 100-fold) up-regulated in S. gordonii monocultures after 3 h growth when exogenous arginine was depleted. Co-cultures without induced coaggregation showed similar regulation. However, within 1 h after coaggregation with A. naeslundii, expression of argC, argG and pyrA_b in S. gordonii was partially up-regulated although arginine was plentiful, and mRNA levels did not increase further when arginine was diminished. Thus, A. naeslundii stabilizes S. gordonii expression of arginine biosynthesis genes in coaggregates but not co-cultures and enables aerobic growth when exogenous arginine is limited.

This article has been cited by other articles:

• Mansour, S., Bailly, J., Landaud, S., Monnet, C., Sarthou, A. S., Cocaign-Bousquet, M., Leroy, S., Irlinger, F., Bonnarme, P. (2009). Investigation of Associations of Yarrowia lipolytica, Staphylococcus xylosus, and Lactococcus lactis in Culture as a First Step in Microbial Interaction Analysis. Appl. Environ. Microbiol. 75: 6422-6430 [Abstract] [Full Text]  
• Nobbs, A. H., Lamont, R. J., Jenkinson, H. F. (2009). Streptococcus Adherence and Colonization. Microbiol. Mol. Biol. Rev. 73: 407-450 [Abstract] [Full Text]  
• Dige, I., Raarup, M. K., Nyengaard, J. R., Kilian, M., Nyvad, B. (2009). Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155: 2116-2126 [Abstract] [Full Text]  
• Herve-Jimenez, L., Guillouard, I., Guedon, E., Boudebbouze, S., Hols, P., Monnet, V., Maguin, E., Rul, F. (2009). Postgenomic Analysis of Streptococcus thermophilus Cocultivated in Milk with Lactobacillus delbrueckii subsp. bulgaricus: Involvement of Nitrogen, Purine, and Iron Metabolism. Appl. Environ. Microbiol. 75: 2062-2073 [Abstract] [Full Text]