title: The Legionella pneumophila kai operon is implicated in stress response and confers fitness in competitive environments.
abstract: Legionella pneumophila uses aquatic protozoa as replication niche and protection from harsh environments. Although L. pneumophila is not known to have a circadian clock, it encodes homologues of the KaiBC proteins of Cyanobacteria that regulate circadian gene expression. We show that L. pneumophila kaiB, kaiC and the downstream gene lpp1114, are transcribed as a unit under the control of the stress sigma factor RpoS. KaiC and KaiB of L. pneumophila do not interact as evidenced by yeast and bacterial two-hybrid analyses. Fusion of the C-terminal residues of cyanobacterial KaiB to Legionella KaiB restores their interaction. In contrast, KaiC of L. pneumophila conserved autophosphorylation activity, but KaiB does not trigger the dephosphorylation of KaiC like in Cyanobacteria. The crystal structure of L. pneumophila KaiB suggests that it is an oxidoreductase-like protein with a typical thioredoxin fold. Indeed, mutant analyses revealed that the kai operon-encoded proteins increase fitness of L. pneumophila in competitive environments, and confer higher resistance to oxidative and sodium stress. The phylogenetic analysis indicates that L. pneumophila KaiBC resemble Synechosystis KaiC2B2 and not circadian KaiB1C1. Thus, the L. pneumophila Kai proteins do not encode a circadian clock, but enhance stress resistance and adaption to changes in the environments.
authors: Institut Pasteur, Biologie des Bactéries Intracellulaires, Paris, France; CNRS UMR 3525, Paris, France.
authors: Maria
authors: M
authors: Loza-Correa
authors: Tobias
authors: T
authors: Sahr
authors: Monica
authors: M
authors: Rolando
authors: Craig
authors: C
authors: Daniels
authors: Pierre
authors: P
authors: Petit
authors: Tania
authors: T
authors: Skarina
authors: Laura
authors: L
authors: Gomez Valero
authors: Delphine
authors: D
authors: Dervins-Ravault
authors: Nadine
authors: N
authors: Honoré
authors: Aleksey
authors: A
authors: Savchenko
authors: Carmen
authors: C
authors: Buchrieser
mesh_terms: D048248:Acanthamoeba castellanii / Q000382:microbiology / Q000502:physiology; D000222:Adaptation, Physiological; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D057906:Circadian Clocks; D056925:Circadian Rhythm Signaling Peptides and Proteins / Q000235:genetics / Q000378:metabolism*; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D056084:Genetic Fitness; D016952:Legionella pneumophila / Q000235:genetics* / Q000502:physiology; D009876:Operon; D010766:Phosphorylation; D010802:Phylogeny; D017434:Protein Structure, Tertiary; D012329:RNA, Bacterial / Q000235:genetics; D013312:Stress, Physiological
chemical_list: D001426:Bacterial Proteins; D056925:Circadian Rhythm Signaling Peptides and Proteins; C114270:KaiB protein, cyanobacteria; C114271:KaiC protein, cyanobacteria; D012329:RNA, Bacterial
references: BMC Genomics. 2008 Apr 13;9:167
references: 18405392
references: Science. 2005 Apr 15;308(5720):414-5
references: 15831759
references: Cell. 2010 Feb 19;140(4):529-39
references: 20178745
references: Nucleic Acids Res. 2009 Jan;37(Database issue):D355-9
references: 18996896
references: Infect Immun. 1997 Jan;65(1):133-43
references: 8975903
references: Nucleic Acids Res. 2010 Jul;38(Web Server issue):W545-9
references: 20457744
references: J Bacteriol. 2010 Feb;192(4):1030-44
references: 20008069
references: Science. 2004 Feb 27;303(5662):1358-61
references: 14988561
references: J Biol Chem. 2005 May 13;280(19):19127-35
references: 15716274
references: Cell Host Microbe. 2013 Apr 17;13(4):395-405
references: 23601102
references: Environ Microbiol. 2013 Feb;15(2):646-62
references: 23033905
references: Cell Microbiol. 2010 Sep 1;12(9):1272-91
references: 20345489
references: FEBS Lett. 1999 Feb 19;445(1):137-43
references: 10069388
references: Proc Natl Acad Sci U S A. 2006 May 30;103(22):8564-9
references: 16707582
references: Microbiol Mol Biol Rev. 1999 Jun;63(2):479-506
references: 10357859
references: Infect Immun. 2002 Jul;70(7):3637-48
references: 12065505
references: Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):495-9
references: 10618446
references: Mol Microbiol. 2002 Apr;44(1):107-18
references: 11967072
references: Trends Microbiol. 2007 Sep;15(9):381-8
references: 17804240
references: Mol Microbiol. 2001 Jun;40(5):1201-14
references: 11401723
references: Structure. 2001 Nov;9(11):1095-106
references: 11709173
references: Adv Genet. 2011;74:13-53
references: 21924974
references: Nat Rev Microbiol. 2009 Oct;7(10):724-35
references: 19756011
references: J Bacteriol. 2000 Dec;182(23):6679-86
references: 11073912
references: Proc Natl Acad Sci U S A. 1998 May 12;95(10):5752-6
references: 9576956
references: FEMS Microbiol Ecol. 2003 Dec 1;46(3):353-7
references: 19719565
references: FEMS Microbiol Rev. 2010 May;34(3):281-94
references: 20132312
references: Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2495-500
references: 12604787
references: J Bacteriol. 2012 Dec;194(24):6828-36
references: 23043001
references: Mol Cell. 2008 Mar 28;29(6):703-16
references: 18342562
references: FEMS Microbiol Lett. 2005 Feb 1;243(1):251-8
references: 15668026
references: Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14805-10
references: 20679240
references: Biometals. 2007 Jun;20(3-4):323-31
references: 17180462
references: Microbiology (Reading). 2008 Jan;154(Pt 1):30-41
references: 18174123
references: FEBS Lett. 2005 Jan 31;579(3):808-12
references: 15670851
references: J Bacteriol. 2010 Jan;192(2):446-55
references: 19915024
references: Genes Dev. 2007 Jan 1;21(1):60-70
references: 17210789
references: Mol Microbiol. 2004 Jul;53(1):29-40
references: 15225301
references: Mol Microbiol. 2010 Apr;76(1):200-19
references: 20199605
references: Infect Immun. 1998 Jul;66(7):3029-34
references: 9632562
references: EMBO J. 1999 Mar 1;18(5):1137-45
references: 10064581
references: Nat Rev Microbiol. 2011 Aug 08;9(10):713-23
references: 21822294
references: Bioinformatics. 2005 May 1;21(9):2104-5
references: 15647292
references: Nat Protoc. 2011 Nov;6(11):1669-82
references: 21979275
references: PLoS Genet. 2010 Feb 19;6(2):e1000851
references: 20174605
references: Curr Biol. 2004 Aug 24;14(16):1481-6
references: 15324665
references: Mol Cell. 2013 Apr 25;50(2):288-94
references: 23541768
references: Microbiology (Reading). 2013 May;159(Pt 5):948-958
references: 23449916
references: Infect Immun. 2003 Aug;71(8):4526-35
references: 12874332
references: Nat Genet. 2004 Nov;36(11):1165-73
references: 15467720
references: J Bacteriol. 2008 May;190(10):3444-55
references: 18359810
references: Science. 2002 Feb 8;295(5557):1073-7
references: 11799204
references: Clin Microbiol Rev. 2010 Apr;23(2):274-98
references: 20375353
references: Methods Mol Biol. 2009;498:297-307
references: 18988033
references: Science. 2007 Nov 2;318(5851):809-12
references: 17916691
references: BMC Genomics. 2011 Nov 01;12:536
references: 22044686
references: J Bacteriol. 2002 Jan;184(1):67-75
references: 11741845
references: Plant Physiol. 2013 Jan;161(1):278-90
references: 23144185
references: N Engl J Med. 1977 Dec 1;297(22):1189-97
references: 335244
references: Photochem Photobiol. 2013 Mar-Apr;89(2):361-9
references: 23025752
references: J Bacteriol. 2006 Sep;188(17):6235-44
references: 16923890
references: Infect Immun. 1989 Jun;57(6):1862-4
references: 2722245
references: Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
references: 15572765
references: Cold Spring Harb Symp Quant Biol. 2007;72:395-404
references: 18419297
references: Front Microbiol. 2010 Dec 06;1:130
references: 21687756
references: N Engl J Med. 1977 Dec 1;297(22):1197-203
references: 335245
references: Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
references: 20124702
references: J Bacteriol. 2012 Mar;194(5):1251-2
references: 22328752
references: J Bacteriol. 1999 Jul;181(13):4118-24
references: 10383985
references: Biopolymers. 1983 Dec;22(12):2577-637
references: 6667333
references: Mol Biol Evol. 2007 Aug;24(8):1596-9
references: 17488738
references: RNA Biol. 2012 Apr;9(4):503-19
references: 22546937
references: J Biol Chem. 2005 Dec 30;280(52):43141-9
references: 16227211
references: Front Microbiol. 2011 Apr 04;2:60
references: 21747786
references: Mol Microbiol. 2009 May;72(3):741-62
references: 19400772
references: Annu Rev Physiol. 2010;72:625-45
references: 20148691
references: Biochemistry. 2011 Sep 27;50(38):8163-71
references: 21851109
references: J Bacteriol. 2001 Mar;183(6):1961-73
references: 11222594
references: Acta Crystallogr D Biol Crystallogr. 1999 Apr;55(Pt 4):849-61
references: 10089316
references: J Bacteriol. 2008 Mar;190(6):1985-96
references: 18192394
references: Infect Immun. 2002 Oct;70(10):5659-69
references: 12228295
references: Biometals. 2006 Apr;19(2):143-57
references: 16718600
references: EMBO J. 2003 May 1;22(9):2127-34
references: 12727879
references: EMBO J. 2007 Sep 5;26(17):4029-37
references: 17717528
references: Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W557-9
references: 15980534
references: Clin Microbiol Rev. 2002 Jul;15(3):506-26
references: 12097254
references: Science. 2005 Jan 14;307(5707):251-4
references: 15550625
references: J Bacteriol. 1996 Mar;178(6):1578-84
references: 8626284
references: Cell Microbiol. 2006 Aug;8(8):1228-40
references: 16882028