Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts.
The quorum sensing (QS) system of Pseudomonas aeruginosa constitutes a sophisticated genome-wide gene regulatory network employing both N-acylhomoserine lactone and 2-alkyl-4-quinolone (AQ) signal molecules. AQ signalling utilizes 2-heptyl-3-hydroxy-4-quinolone (PQS) and its immediate precursor, 2-heptyl-4-quinolone (HHQ). AQ biosynthesis requires the first four genes of the pqsABCDE operon and while the biochemical function of pqsE is not known, it is required for the production of secondary metabolites such as pyocyanin. To gain insights into the relationship between the AQ stimulon, the PqsE stimulon and the regulatory function of PqsE, we constructed a pqsE inducible mutant (pqsEind) and compared the transcriptomes of the induced and uninduced states with a pqsA mutant. Of 158 genes exhibiting altered expression in the pqsA mutant, 51% were also affected in the pqsE mutant. Following induction of pqsE, 237 genes were differentially expressed compared with the wild-type strain. In the pqsEind strain, pqsA was highly expressed but following induction both pqsA expression and AQ biosynthesis were repressed, revealing a negative autoregulatory role for PqsE. Furthermore, pqsE was required for swarming motility and virulence in plant and animal infection models in the absence of AQs, while mature biofilm development required both pqsA and pqsE. Taken together these data reveal that PqsE is a key regulator within the QS circuitry facilitating the environmental adaptation of P. aeruginosa.
Rampioni
Giordano
G
School of Molecular Medical Sciences, Centre for Biomolecular Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK.
Pustelny
Christian
C
Fletcher
Matthew P
MP
Wright
Victoria J
VJ
Bruce
Mary
M
Rumbaugh
Kendra P
KP
Heeb
Stephan
S
Cámara
Miguel
M
Williams
Paul
P
D000222:Adaptation, Physiological; D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D018441:Biofilms / Q000254:growth & development; D004777:Environment; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D006801:Humans; D046228:Microarray Analysis; D015394:Molecular Structure; D009876:Operon; D010944:Plants / Q000382:microbiology; D011550:Pseudomonas aeruginosa / Q000472:pathogenicity / Q000502:physiology*; D011710:Pyocyanine / Q000378:metabolism; D015363:Quinolones / Q000737:chemistry / Q000378:metabolism*; D053038:Quorum Sensing / Q000502:physiology; D015398:Signal Transduction / Q000502:physiology
C407944:2-heptyl-3-hydroxy-4-quinolone; D001426:Bacterial Proteins; D015363:Quinolones; D011710:Pyocyanine
J Bacteriol. 2001 Dec;183(24):7044-52
11717261
Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6911-6
11381121
Biochemistry. 2009 Nov 3;48(43):10298-307
19788310
J Bacteriol. 2007 Jul;189(13):4827-36
17449617
J Biol Chem. 2008 Oct 24;283(43):28788-94
18728009
J Bacteriol. 1996 Mar;178(5):1310-9
8631707
PLoS Pathog. 2008 Sep 26;4(9):e1000166
18818733
FEMS Microbiol Lett. 2004 Jan 15;230(1):27-34
14734162
J Bacteriol. 2008 Feb;190(4):1247-55
18083812
Gene. 2001 Jan 10;262(1-2):147-53
11179678
J Bacteriol. 2008 Dec;190(24):7947-56
18931133
Cell Microbiol. 2006 Dec;8(12):1841-9
17026480
Mol Microbiol. 2007 Dec;66(6):1557-65
18045385
Biotechniques. 2000 Nov;29(5):948-50, 952
11084852
Mol Microbiol. 2003 Oct;50(1):29-43
14507361
J Bacteriol. 2008 Nov;190(21):7043-51
18776012
Environ Microbiol. 2007 Nov;9(11):2683-93
17922753
J Bacteriol. 2005 Jun;187(11):3630-5
15901684
Mol Microbiol. 2005 Feb;55(4):998-1014
15686549
J Bacteriol. 2000 Nov;182(22):6401-11
11053384
FEMS Microbiol Lett. 2005 Dec 1;253(1):103-9
16239083
J Bacteriol. 2002 Dec;184(23):6472-80
12426334
Gene. 1992 Nov 2;121(1):47-54
1427098
J Biol Chem. 2008 Jun 6;283(23):15558-67
18424436
Antimicrob Agents Chemother. 2009 Nov;53(11):4891-7
19721066
Nat Rev Microbiol. 2007 May;5(5):363-75
17435791
J Bacteriol. 2001 Nov;183(21):6454-65
11591691
Curr Opin Microbiol. 2009 Apr;12(2):182-91
19249239
Proc Natl Acad Sci U S A. 1990 Jun;87(12):4645-9
2162051
Mol Microbiol. 2009 Sep;73(6):1072-85
19682264
J Bacteriol. 2000 May;182(10):2702-8
10781536
Eur J Biochem. 1971 Feb 1;18(3):391-400
5542949
Trends Microbiol. 2008 Oct;16(10):496-506
18775660
Nature. 2005 Sep 15;437(7057):422-5
16163359
J Bacteriol. 2005 Jul;187(13):4372-80
15968046
J Bacteriol. 2006 Jan;188(2):815-9
16385073
Annu Rev Microbiol. 2002;56:289-314
12142488
Environ Microbiol. 2008 Sep;10(9):2331-43
18485000
J Bacteriol. 2004 May;186(10):2936-45
15126453
Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1339-44
14739337
Microbiology (Reading). 2009 Mar;155(Pt 3):712-723
19246742
Chem Biol. 2007 Jan;14(1):87-96
17254955
Curr Biol. 2009 Feb 24;19(4):341-5
19230668
Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11229-34
10500159
Mol Microbiol. 2008 Jul;69(2):491-502
18630345
Microbiology (Reading). 2006 Jun;152(Pt 6):1679-1686
16735731
EMBO J. 2003 Aug 1;22(15):3803-15
12881415
Infect Immun. 2005 May;73(5):2958-66
15845502
WormBook. 2006 Feb 11;:1-11
18050451
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14613-8
11724939
Microbiology (Reading). 2004 Nov;150(Pt 11):3797-3806
15528665
J Bacteriol. 2003 Apr;185(7):2080-95
12644477
Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11076-81
16043697
Trends Mol Med. 2004 Dec;10(12):599-606
15567330
Mol Microbiol. 2006 Dec;62(6):1689-99
17083468
Environ Microbiol. 2006 Jun;8(6):1095-104
16689730
Environ Microbiol. 2006 Aug;8(8):1318-29
16872396
Microbiology (Reading). 2005 Apr;151(Pt 4):1113-1125
15817779
J Bacteriol. 2002 Dec;184(23):6481-9
12426335
Nat Protoc. 2009;4(2):117-24
19180083
J Bacteriol. 2003 Apr;185(7):2066-79
12644476
Microbiology (Reading). 2007 May;153(Pt 5):1318-1328
17464046
Trends Microbiol. 2003 May;11(5):195-200
12781517
Mol Microbiol. 2006 Sep;61(5):1308-21
16879411
Mol Microbiol. 2006 Feb;59(4):1114-28
16430688
FEMS Microbiol Lett. 1990 Jul;58(2):221-5
2121587
Infect Immun. 2007 Aug;75(8):3715-21
17562773
Gene. 1991 Jan 2;97(1):109-21
1899844