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Journal of Bacteriology, February 2009, p. 1044-1055, Vol. 191, No. 3
0021-9193/09/$08.00+0     doi:10.1128/JB.01270-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Response of Porphyromonas gingivalis to Heme Limitation in Continuous Culture{triangledown} ,{dagger}

Stuart G. Dashper,1,{ddagger} Ching-Seng Ang,1,{ddagger} Paul D. Veith,1 Helen L. Mitchell,1 Alvin W. H. Lo,1 Christine A. Seers,1 Katrina A. Walsh,1 Nada Slakeski,1 Dina Chen,1 J. Patricia Lissel,1 Catherine A. Butler,1 Neil M. O'Brien-Simpson,1 Ian G. Barr,2 and Eric C. Reynolds1*

Cooperative Research Centre for Oral Health Science, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Victoria, Australia,1 WHO Collaborating Centre for Reference and Research on Influenza, Parkville, Victoria, Australia2

Received 10 September 2008/ Accepted 13 November 2008

Porphyromonas gingivalis is an anaerobic, asaccharolytic, gram-negative bacterium that has essential requirements for both iron and protoporphyrin IX, which it preferentially obtains as heme. A combination of large-scale quantitative proteomic analysis using stable isotope labeling strategies and mass spectrometry, together with transcriptomic analysis using custom-made DNA microarrays, was used to identify changes in P. gingivalis W50 protein and transcript abundances on changing from heme-excess to heme-limited continuous culture. This approach identified 160 genes and 70 proteins that were differentially regulated by heme availability, with broad agreement between the transcriptomic and proteomic data. A change in abundance of the enzymes of the aspartate and glutamate catabolic pathways was observed with heme limitation, which was reflected in organic acid end product levels of the culture fluid. These results demonstrate a shift from an energy-efficient anaerobic respiration to a less efficient process upon heme limitation. Heme limitation also resulted in an increase in abundance of a protein, PG1374, which we have demonstrated, by insertional inactivation, to have a role in epithelial cell invasion. The greater abundance of a number of transcripts/proteins linked to invasion of host cells, the oxidative stress response, iron/heme transport, and virulence of the bacterium indicates that there is a broad response of P. gingivalis to heme availability.

* Corresponding author. Mailing address: Centre for Oral Health Science, Melbourne Dental School, The University of Melbourne, 720 Swanston Street, Victoria 3010, Australia. Phone: 61 3 9341 1547. Fax: 61 3 9341 1596. E-mail: e.reynolds{at}unimelb.edu.au

{triangledown} Published ahead of print on 21 November 2008.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

{ddagger} S.G.D. and C.-S.A. contributed equally to this work.

Journal of Bacteriology, February 2009, p. 1044-1055, Vol. 191, No. 3
0021-9193/09/$08.00+0     doi:10.1128/JB.01270-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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