Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate.
Porphyromonas gingivalis, previously classified as a strict anaerobe, can grow in the presence of low concentrations of oxygen. Microarray analysis revealed alteration in gene expression in the presence of 6 % oxygen. During the exponential growth phase, 96 genes were upregulated and 79 genes were downregulated 1.4-fold. Genes encoding proteins that play a role in oxidative stress protection were upregulated, including alkyl hydroperoxide reductase (ahpCF), superoxide dismutase (sod) and thiol peroxidase (tpx). Significant changes in gene expression of proteins that mediate oxidative metabolism, such as cytochrome d ubiquinol oxidase-encoding genes, cydA and cydB, were detected. The expression of genes encoding formate uptake transporter (PG0209) and formate tetrahydrofolate ligase (fhs) was drastically elevated, which indicates that formate metabolism plays a major role under aerobic conditions. The concomitant reduction of expression of a gene encoding the lactate transporter PG1340 suggests decreased utilization of this nutrient. The concentrations of both formate and lactate were assessed in culture supernatants and cells, and they were in agreement with the results obtained at the transcriptional level. Also, genes encoding gingipain protease secretion/maturation regulator (porR) and protease transporter (porT) had reduced expression in the presence of oxygen, which also correlated with reduced protease activities under aerobic conditions. In addition, metal transport was affected, and while iron-uptake genes such as the genes encoding the haemin uptake locus (hmu) were downregulated, expression of manganese transporter genes, such as feoB2, was elevated in the presence of oxygen. Finally, genes encoding putative regulatory proteins such as extracellular function (ECF) sigma factors as well as small proteins had elevated expression levels in the presence of oxygen. As P. gingivalis is distantly related to the well-studied model organism Escherichia coli, results from our work may provide further understanding of oxygen metabolism and protection in other related bacteria belonging to the phylum Bacteroidetes.
Lewis
Janina P
JP
Department of Biochemistry and Molecular Biology, Virginia Commonwealth University, Richmond, VA, USA.|Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, VA, USA.|The Philips Institute of Oral and Craniofacial Molecular Biology, Virginia Commonwealth University, Richmond, VA, USA.
Iyer
Divya
D
The Philips Institute of Oral and Craniofacial Molecular Biology, Virginia Commonwealth University, Richmond, VA, USA.
Anaya-Bergman
Cecilia
C
University of San Luis, San Luis, Argentina.|The Philips Institute of Oral and Craniofacial Molecular Biology, Virginia Commonwealth University, Richmond, VA, USA.
D019295:Computational Biology; D003470:Culture Media; D005561:Formates / Q000378:metabolism*; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D005798:Genes, Bacterial; D016680:Genome, Bacterial; D019344:Lactic Acid / Q000378:metabolism*; D020411:Oligonucleotide Array Sequence Analysis; D010100:Oxygen / Q000378:metabolism*; D016966:Porphyromonas gingivalis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*
D003470:Culture Media; D005561:Formates; D019344:Lactic Acid; D010100:Oxygen
Crit Rev Oral Biol Med. 1999;10(4):487-503
10634585
J Clin Microbiol. 1992 Feb;30(2):418-26
1537912
Microbiology (Reading). 2002 Apr;148(Pt 4):1183-1191
11932462
Oral Microbiol Immunol. 2000 Dec;15(6):341-9
11154429
J Dent Res. 1990 Sep;69(9):1567-72
2204641
Biochem Biophys Res Commun. 1993 Nov 30;197(1):241-7
7902712
J Med Microbiol. 1980 Feb;13(1):89-101
6102159
J Bacteriol. 2003 Sep;185(18):5591-601
12949112
Bioessays. 1996 Jan;18(1):55-62
8593164
Microbiology (Reading). 2006 Nov;152(Pt 11):3367-3382
17074906
J Biol Chem. 1982 Feb 25;257(4):1980-6
6799517
Structure. 2008 Jul;16(7):1105-15
18611383
Microbiology (Reading). 1996 Apr;142 ( Pt 4):755-763
8936304
J Clin Periodontol. 1986 Nov;13(10):912-7
3466908
Appl Environ Microbiol. 1979 Jun;37(6):1206-10
16345401
Oral Microbiol Immunol. 1992 Oct;7(5):304-8
1494455
Mol Microbiol. 2008 Sep;69(5):1153-64
18573179
Free Radic Res. 1997 Feb;26(2):145-57
9257126
Infect Immun. 2003 Mar;71(3):1170-8
12595429
J Bacteriol. 1988 Feb;170(2):995-7
3257484
J Clin Periodontol. 1992 Jan;19(1):35-42
1346265
J Bacteriol. 2000 Oct;182(20):5813-22
11004182
Oral Microbiol Immunol. 2008 Aug;23(4):308-14
18582330
Mol Microbiol. 2005 May;56(3):811-23
15819634
Ann Periodontol. 1998 Jul;3(1):127-41
9722697
Nature. 2004 Jan 29;427(6973):441-4
14749831
Arch Biochem Biophys. 2000 Jan 1;373(1):1-6
10620317
Mol Microbiol. 2002 Jul;45(2):365-74
12123450
J Med Chem. 1989 Aug;32(8):1949-58
2754716
Microbiology (Reading). 2009 Feb;155(Pt 2):328-337
19202082
J Dent Res. 2008 Nov;87(11):1004-15
18946006
J Biol Chem. 1980 Mar 10;255(5):1885-90
7354066
Mol Microbiol. 2000 Dec;38(5):1061-73
11123679
Proc Natl Acad Sci U S A. 1990 Jan;87(1):394-8
2153299
J Periodontal Res. 2004 Feb;39(1):1-9
14687221
Proc Natl Acad Sci U S A. 2004 Nov 30;101(48):16917-22
15546975
J Clin Periodontol. 2003 Sep;30(9):761-72
12956651
Oral Microbiol Immunol. 2004 Apr;19(2):88-94
14871347
Biochem Biophys Res Commun. 1997 Apr 28;233(3):848-52
9168946
Oral Microbiol Immunol. 1991 Apr;6(2):76-80
1945491
J Bacteriol. 1988 Jul;170(7):3255-61
2838464
Appl Environ Microbiol. 1990 Jun;56(6):1944-8
2166474
Periodontol 2000. 2003;32:24-35
12756031
Oral Oncol. 1998 Jul;34(4):304-8
9813727
J Biol Chem. 2005 Mar 11;280(10):8668-77
15634642
Biochem J. 2000 Jan 15;345 Pt 2:345-50
10620511
J Bacteriol. 2007 Nov;189(22):8015-23
17873045
FEBS Lett. 1997 Apr 21;407(1):32-6
9141476
Oral Microbiol Immunol. 2004 Jun;19(3):137-43
15107063
Microbiol Mol Biol Rev. 1998 Dec;62(4):1244-63
9841671
J Bacteriol. 1994 Apr;176(7):1939-43
8144460
Crit Rev Oral Biol Med. 2001;12(3):192-216
11497373
Microbiology (Reading). 2000 May;146 ( Pt 5):1119-1127
10832639
Gene. 1990 Nov 30;96(1):149-50
2265754
Microbiology (Reading). 2006 Apr;152(Pt 4):955-966
16549660
Infect Immun. 1999 May;67(5):2619-23
10225930
Infect Immun. 2006 May;74(5):3002-5
16622239
Arch Biochem Biophys. 2005 Jan 1;433(1):212-26
15581578
J Bacteriol. 2006 Apr;188(7):2454-62
16547032
Infect Immun. 2006 Jul;74(7):4214-23
16790796
Eur J Oral Sci. 2005 Feb;113(1):14-9
15693824
Infect Immun. 1998 Jul;66(7):3035-42
9632563
Arch Biochem Biophys. 1982 Apr 1;214(2):452-63
6284026
DNA Res. 2008 Aug;15(4):215-25
18524787
J Bacteriol. 2000 Sep;182(17):4704-10
10940008
Curr Diab Rep. 2004 Feb;4(1):46-50
14764280
J Bacteriol. 2008 Feb;190(4):1436-46
18065546
Infect Immun. 2005 Jul;73(7):3983-9
15972485
J Bacteriol. 2007 Aug;189(16):6080-4
17557822
Mol Microbiol. 1997 Aug;25(3):605-15
9302022
Infect Immun. 1996 Oct;64(10):4000-7
8926061
J Clin Periodontol. 1993 May;20(5):340-5
8388896
J Periodontol. 2007 May;78(5):833-41
17470016
J Biol Chem. 2005 Jul 29;280(30):28095-102
15901729
Mol Microbiol. 2007 May;64(4):1061-74
17501928
Curr Opin Dent. 1992 Mar;2:5-11
1520938