title: Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa.
abstract: Pyoverdine is the primary siderophore of the gram-negative bacterium Pseudomonas aeruginosa. The pyoverdine region was recently identified as the most divergent locus alignable between strains in the P. aeruginosa genome. Here we report the nucleotide sequence and analysis of more than 50 kb in the pyoverdine region from nine strains of P. aeruginosa. There are three divergent sequence types in the pyoverdine region, which correspond to the three structural types of pyoverdine. The pyoverdine outer membrane receptor fpvA may be driving diversity at the locus: it is the most divergent alignable gene in the region, is the only gene that showed substantial intratype variation that did not appear to be generated by recombination, and shows evidence of positive selection. The hypothetical membrane protein PA2403 also shows evidence of positive selection; residues on one side of the membrane after protein folding are under positive selection. R', previously identified as a type IV strain, is clearly derived from a type III strain via a 3.4-kb deletion which removes one amino acid from the pyoverdine side chain peptide. This deletion represents a natural modification of the product of a nonribosomal peptide synthetase enzyme, whose consequences are predictive from the DNA sequence. There is also linkage disequilibrium between the pyoverdine region and pvdY, a pyoverdine gene separated by 30 kb from the pyoverdine region. The pyoverdine region shows evidence of horizontal transfer; we propose that some alleles in the region were introduced from other soil bacteria and have been subsequently maintained by diversifying selection.
authors.affiliation: Program of Molecular and Cellular Biology, University of Washington, Seattle, WA 98195, USA. smithee@u.washington.edu
authors.forename: Eric E
authors.initials: EE
authors.lastname: Smith
authors.forename: Elizabeth H
authors.initials: EH
authors.lastname: Sims
authors.forename: David H
authors.initials: DH
authors.lastname: Spencer
authors.forename: Rajinder
authors.initials: R
authors.lastname: Kaul
authors.forename: Maynard V
authors.initials: MV
authors.lastname: Olson
mesh_terms: D001425:Bacterial Outer Membrane Proteins / Q000235:genetics; D001426:Bacterial Proteins / Q000235:genetics; D003001:Cloning, Molecular; D014644:Genetic Variation; D007536:Isomerism; D015810:Linkage Disequilibrium; D009842:Oligopeptides / Q000737:chemistry / Q000235:genetics*; D046908:Peptide Biosynthesis, Nucleic Acid-Independent / Q000502:physiology; D010453:Peptide Synthases / Q000235:genetics; D011550:Pseudomonas aeruginosa / Q000235:genetics*; D011995:Recombination, Genetic / Q000502:physiology; D017262:Siderophores / Q000235:genetics
chemical_list: D001425:Bacterial Outer Membrane Proteins; D001426:Bacterial Proteins; C082326:FpvA protein, Pseudomonas aeruginosa; D009842:Oligopeptides; D017262:Siderophores; C042453:pyoverdin; D010453:Peptide Synthases; C091136:pyoverdine synthetase protein, Pseudomonas
references.citation: J Bacteriol. 2003 May;185(9):2848-55
references.pmid: 12700264
references.citation: Trends Microbiol. 2003 May;11(5):195-200
references.pmid: 12781517
references.citation: FEMS Microbiol Rev. 2003 Jun;27(2-3):215-37
references.pmid: 12829269
references.citation: Genetics. 2003 Jul;164(3):1229-36
references.pmid: 12871927
references.citation: Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10181-6
references.pmid: 12928499
references.citation: Nucleic Acids Res. 2004 Jan 1;32(Database issue):D138-41
references.pmid: 14681378
references.citation: J Bacteriol. 2004 Jan;186(2):518-34
references.pmid: 14702321
references.citation: Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2530-5
references.pmid: 14983043
references.citation: J Bacteriol. 2004 Apr;186(7):2115-22
references.pmid: 15028697
references.citation: Methods Mol Biol. 2000;132:365-86
references.pmid: 10547847
references.citation: Mol Microbiol. 1999 Nov;34(3):399-413
references.pmid: 10564483
references.citation: Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):15202-7
references.pmid: 10611362
references.citation: Chem Biol. 2000 Mar;7(3):211-24
references.pmid: 10712928
references.citation: Infect Immun. 2000 Apr;68(4):1834-9
references.pmid: 10722571
references.citation: Genetics. 2000 May;155(1):431-49
references.pmid: 10790415
references.citation: J Bacteriol. 2000 Jun;182(11):3125-35
references.pmid: 10809691
references.citation: Trends Genet. 2000 Jun;16(6):276-7
references.pmid: 10827456
references.citation: Protein Sci. 2000 Jun;9(6):1162-76
references.pmid: 10892809
references.citation: Nature. 2000 Aug 31;406(6799):959-64
references.pmid: 10984043
references.citation: Annu Rev Microbiol. 2000;54:881-941
references.pmid: 11018148
references.citation: Arch Microbiol. 2000 Sep;174(3):135-42
references.pmid: 11041343
references.citation: Plant Physiol. 2000 Dec;124(4):1766-74
references.pmid: 11115892
references.citation: J Infect Dis. 2001 Feb 1;183(3):444-52
references.pmid: 11133376
references.citation: Nucleic Acids Res. 1992 Mar 11;20(5):1083-5
references.pmid: 1549470
references.citation: FEMS Microbiol Rev. 1993 Apr;10(3-4):209-28
references.pmid: 8318257
references.citation: J Bacteriol. 1993 Aug;175(15):4597-604
references.pmid: 8335619
references.citation: Nucleic Acids Res. 1994 Nov 11;22(22):4673-80
references.pmid: 7984417
references.citation: Annu Rev Microbiol. 1994;48:619-54
references.pmid: 7826021
references.citation: Science. 1995 Jun 30;268(5219):1899-902
references.pmid: 7604262
references.citation: Infect Immun. 1996 Feb;64(2):518-23
references.pmid: 8550201
references.citation: Nucleic Acids Res. 1997 Jan 15;25(2):451-2
references.pmid: 9016579
references.citation: Microbiology. 1997 Jan;143 ( Pt 1):35-43
references.pmid: 9025276
references.citation: Proc Natl Acad Sci U S A. 1997 May 13;94(10):5225-30
references.pmid: 9144219
references.citation: Comput Appl Biosci. 1997 Oct;13(5):555-6
references.pmid: 9367129
references.citation: Nucleic Acids Res. 1998 Feb 15;26(4):1107-15
references.pmid: 9461475
references.citation: Nucleic Acids Res. 1998 Jun 15;26(12):2971-80
references.pmid: 9611243
references.citation: Science. 1998 Dec 18;282(5397):2215-20
references.pmid: 9856937
references.citation: Nat Struct Biol. 1999 Jan;6(1):56-63
references.pmid: 9886293
references.citation: FEMS Microbiol Lett. 1999 Jan 1;170(1):145-50
references.pmid: 9919663
references.citation: J Bacteriol. 1999 Jun;181(12):3849-51
references.pmid: 10368165
references.citation: Can J Microbiol. 1957 Jun;3(4):611-25
references.pmid: 13437224
references.citation: J Bacteriol. 2001 Feb;183(3):843-53
references.pmid: 11208781
references.citation: Genome Res. 2001 Apr;11(4):614-25
references.pmid: 11282977
references.citation: Genome Res. 2002 Jan;12(1):190-7
references.pmid: 11779844
references.citation: Arch Biochem Biophys. 2002 Jan 15;397(2):179-83
references.pmid: 11795869
references.citation: Z Naturforsch C. 2001 Nov-Dec;56(11-12):933-8
references.pmid: 11837678
references.citation: Science. 2002 Mar 1;295(5560):1715-9
references.pmid: 11872840
references.citation: Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3159-64
references.pmid: 11867744
references.citation: J Bacteriol. 2002 Jul;184(13):3614-22
references.pmid: 12057956
references.citation: Mol Microbiol. 2002 Sep;45(5):1177-90
references.pmid: 12207687
references.citation: Mol Microbiol. 2002 Sep;45(5):1277-87
references.pmid: 12207696
references.citation: Chembiochem. 2002 Jun 3;3(6):490-504
references.pmid: 12325005
references.citation: J Bacteriol. 2002 Dec;184(23):6665-80
references.pmid: 12426355
references.citation: Microbiology. 2002 Nov;148(Pt 11):3497-509
references.pmid: 12427941
references.citation: Nucleic Acids Res. 2003 Jan 1;31(1):383-7
references.pmid: 12520028
references.citation: Microbiology. 2004 Jun;150(Pt 6):1671-80
references.pmid: 15184553
references.citation: Chem Biol. 2004 Jul;11(7):971-80
references.pmid: 15271355
references.citation: Nature. 2004 Aug 26;430(7003):1024-7
references.pmid: 15329720
references.citation: J Mol Biol. 1982 May 5;157(1):105-32
references.pmid: 7108955
references.citation: Nucleic Acids Res. 1987 Feb 11;15(3):1281-95
references.pmid: 3547335
references.citation: Gene. 1987;57(2-3):267-72
references.pmid: 3319781
references.citation: Infect Immun. 1989 Nov;57(11):3491-7
references.pmid: 2509364
references.citation: Methods Enzymol. 1991;194:3-21
references.pmid: 2005794
references.citation: Methods Enzymol. 1991;204:63-113
references.pmid: 1943786
references.citation: Environ Microbiol. 2002 Dec;4(12):787-98
references.pmid: 12534462
references.citation: Environ Microbiol. 2002 Dec;4(12):799-808
references.pmid: 12534463
references.citation: Environ Microbiol. 2002 Dec;4(12):898-911
references.pmid: 12534471
references.citation: J Bacteriol. 2003 Feb;185(4):1316-25
references.pmid: 12562802
references.citation: Genome Res. 2003 Feb;13(2):145-58
references.pmid: 12566393
references.citation: Proc Biol Sci. 2003 Jan 7;270(1510):37-44
references.pmid: 12590769
references.citation: Microbiology. 2003 Apr;149(Pt 4):821-31
references.pmid: 12686625
references.citation: Front Biosci. 2003 May 1;8:d661-86
references.pmid: 12700066