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Universal soldier: Pseudomonas aeruginosa – an opportunistic generalist |
Jeremy GROSS1, Ian J. PASSMORE1, Jade C. S. CHUNG1, Olena RZHEPISHEVSKA2, Madeleine RAMSTEDT2, Martin WELCH1( ) |
1. Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, UK; 2. Department of Chemistry, Ume? University, Ume? 901 87, Sweden |
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Abstract The opportunistic pathogen Pseudomonas aeruginosa commonly causes chronic and ultimately deadly lung infections in individuals with the genetic disease cystic fibrosis (CF). P. aeruginosa is metabolically diverse; it displays a remarkable ability to adapt to and successfully occupy almost any niche, including the ecologically complex CF lung. These P. aeruginosa lung infections are a fascinating example of microbial evolution within a “natural” ecosystem. Initially, P. aeruginosa shares the lung niche with a plethora of other microorganisms and is vulnerable to antibiotic challenges. Over time, adaptive evolution leads to certain commonly-observed phenotypic changes within the P. aeruginosa population, some of which render it resistant to antibiotics and apparently help it to out-compete the other species that co-habit the airways. Improving genomics techniques continue to elucidate the evolutionary mechanisms of P. aeruginosa within the CF lung and will hopefully identify new vulnerabilities in this robust and versatile pathogen.
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Keywords
Pseudomonas aeruginosa
cystic fibrosis
evolution
adaptive radiation
antibiotic resistance
quorum sensing
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Corresponding Author(s):
WELCH Martin,Email:mw240@cam.ac.uk
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Issue Date: 01 August 2013
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1 |
Bjarnsholt T, Jensen P ?, Jakobsen T H, Phipps R, Nielsen A K, Rybtke M T, Tolker-Nielsen T, Givskov M, H?iby N, Ciofu O (2010). Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS ONE , 5(4): e10115 doi: 10.1371/journal.pone.0010115
|
2 |
Brockhurst M A, Colegrave N, Hodgson D J, Buckling A (2007). Niche occupation limits adaptive radiation in experimental microcosms. PLoS ONE , 2(2): e193 doi: 10.1371/journal.pone.0000193
|
3 |
Buckling A, Wills M A, Colegrave N (2003). Adaptation limits diversification of experimental bacterial populations. Science , 302(5653): 2107–2109 doi: 10.1126/science.1088848
|
4 |
Chugani S, Kim B S, Phattarasukol S, Brittnacher M J, Choi S H, Harwood C S, Greenberg E P (2012). Strain-dependent diversity in the Pseudomonas aeruginosa quorum-sensing regulon. Proc Natl Acad Sci USA , 109(41): E2823–E2831 doi: 10.1073/pnas.1214128109
|
5 |
Chung J C S, Becq J, Fraser L, Schulz-Trieglaff O, Bond N J, Foweraker J, Bruce K D, Smith G P, Welch M (2012). Genomic variation among contemporary Pseudomonas aeruginosa isolates from chronically infected cystic fibrosis patients. J Bacteriol , 194(18): 4857–4866 doi: 10.1128/JB.01050-12
|
6 |
Collier D N, Anderson L, McKnight S L, Noah T L, Knowles M, Boucher R, Schwab U, Gilligan P, Pesci E C (2002). A bacterial cell to cell signal in the lungs of cystic fibrosis patients. FEMS Microbiol Lett , 215(1): 41–46 doi: 10.1111/j.1574-6968.2002.tb11367.x
|
7 |
Cox M J, Allgaier M, Taylor B, Baek M S, Huang Y J, Daly R A, Karaoz U, Andersen G L, Brown R, Fujimura K E, Wu B, Tran D, Koff J, Kleinhenz M E, Nielson D, Brodie E L, Lynch S V (2010). Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS ONE , 5(6): e11044 doi: 10.1371/journal.pone.0011044
|
8 |
Cramer N, Klockgether J, Wrasman K, Schmidt M, Davenport C F, Tümmler B (2011). Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol , 13(7): 1690–1704 doi: 10.1111/j.1462-2920.2011.02483.x
|
9 |
Daniels T W V, Rogers G B, Stressmann F A, van der Gast C J, Bruce K D, Jones G R, Connett G J, Legg J P, Carroll M P (2013). Impact of antibiotic treatment for pulmonary exacerbations on bacterial diversity in cystic fibrosis. J Cyst Fibros , 12(1): 22–28 doi: 10.1016/j.jcf.2012.05.008
|
10 |
Diggle S P, Griffin A S, Campbell G S, West S A (2007). Cooperation and conflict in quorum-sensing bacterial populations. Nature , 450(7168): 411–414 doi: 10.1038/nature06279
|
11 |
Foweraker J (2009). Recent advances in the microbiology of respiratory tract infection in cystic fibrosis. Br Med Bull , 89(1): 93–110 doi: 10.1093/bmb/ldn050
|
12 |
Govan J R, Deretic V (1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev , 60: 539–574
|
13 |
Guss A M, Roeselers G, Newton I L G, Young C R, Klepac-Ceraj V, Lory S, Cavanaugh C M (2011). Phylogenetic and metabolic diversity of bacteria associated with cystic fibrosis. ISME J , 5(1): 20–29 doi: 10.1038/ismej.2010.88
|
14 |
Hardin G (1960). The competitive exclusion principle. Science , 131(3409): 1292–1297 doi: 10.1126/science.131.3409.1292
|
15 |
H?ussler S, Tümmler B, Weissbrodt H, Rohde M, Steinmetz I (1999). Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis , 29(3): 621–625 doi: 10.1086/598644
|
16 |
H?ussler S, Ziegler I, L?ttel A, von G?tz F, Rohde M, Wehmh?hner D, Saravanamuthu S, Tümmler B, Steinmetz I (2003). Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol , 52(4): 295–301 doi: 10.1099/jmm.0.05069-0
|
17 |
Hobbs E C, Fontaine F, Yin X, Storz G (2011). An expanding universe of small proteins. Curr Opin Microbiol , 14(2): 167–173 doi: 10.1016/j.mib.2011.01.007
|
18 |
Jacobs M A, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Liu C R, Guenthner D, Bovee D, Olson M V, Manoil C (2003). Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci USA , 100(24): 14339–14344 doi: 10.1073/pnas.2036282100
|
19 |
James C E, Fothergill J L, Kalwij H, Hall A J, Cottell J, Brockhurst M A, Winstanley C (2012). Differential infection properties of three inducible prophages from an epidemic strain of Pseudomonas aeruginosa. BMC Microbiol , 12(1): 216 doi: 10.1186/1471-2180-12-216
|
20 |
Klockgether J, Miethke N, Kubesch P, Bohn Y S, Brockhausen I, Cramer N, Eberl L, Greipel J, Herrmann C, Herrmann S, Horatzek S, Lingner M, Luciano L, Salunkhe P, Schomburg D, Wehsling M, Wiehlmann L, Davenport C F, Tümmler B (2013). Intraclonal diversity of the Pseudomonas aeruginosa cystic fibrosis airway isolates TBCF10839 and TBCF121838: distinct signatures of transcriptome, proteome, metabolome, adherence and pathogenicity despite an almost identical genome sequence. Environ Microbiol , 15(1): 191–210 doi: 10.1111/j.1462-2920.2012.02842.x
|
21 |
Kumar A, Schweizer H P (2005). Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv Drug Deliv Rev , 57(10): 1486–1513 doi: 10.1016/j.addr.2005.04.004
|
22 |
Lorè N I, Cigana C, De Fino I, Riva C, Juhas M, Schwager S, Eberl L, Bragonzi A (2012). Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS ONE , 7(4): e35648 doi: 10.1371/journal.pone.0035648
|
23 |
MacLean R C (2005). Adaptive radiation in microbial microcosms. J Evol Biol , 18(6): 1376–1386 doi: 10.1111/j.1420-9101.2005.00931.x
|
24 |
MacLean R C, Bell G, Rainey P B (2004). The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proc Natl Acad Sci USA , 101(21): 8072–8077 doi: 10.1073/pnas.0307195101
|
25 |
Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish J M, Koehrsen M, Rokas A, Yandava C N, Engels R, Zeng E, Olavarietta R, Doud M, Smith R S, Montgomery P, White J R, Godfrey P A, Kodira C, Birren B, Galagan J E, Lory S (2008). Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci USA , 105(8): 3100–3105 doi: 10.1073/pnas.0711982105
|
26 |
Mowat E, Paterson S, Fothergill J L, Wright E A, Ledson M J, Walshaw M J, Brockhurst M A, Winstanley C (2011). Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med , 183(12): 1674–1679 doi: 10.1164/rccm.201009-1430OC
|
27 |
Oliver A, Cantón R, Campo P, Baquero F, Blázquez J (2000). High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science , 288(5469): 1251–1253 doi: 10.1126/science.288.5469.1251
|
28 |
Pritt B, O’Brien L, Winn W (2007). Mucoid Pseudomonas in cystic fibrosis. Am J Clin Pathol , 128(1): 32–34 doi: 10.1309/KJRPC7DD5TR9NTDM
|
29 |
Rainey P B, Travisano M (1998). Adaptive radiation in a heterogeneous environment. Nature , 394(6688): 69–72 doi: 10.1038/27900
|
30 |
Rau M H, Marvig L R, Ehrlich G D, Molin S, Jelsbak L (2012). Deletion and acquisition of genomic content during early stage adaptation of Pseudomonas aeruginosa to a human host environment. Environ Microbiol , 14(8): 2200–2211 doi: 10.1111/j.1462-2920.2012.02795.x
|
31 |
Rogers G B, Carroll M P, Serisier D J, Hockey P M, Jones G, Bruce K D (2004). Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16s ribosomal DNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol , 42(11): 5176–5183 doi: 10.1128/JCM.42.11.5176-5183.2004
|
32 |
Rogers G B, Hart C A, Mason J R, Hughes M, Walshaw M J, Bruce K D (2003). Bacterial diversity in cases of lung infection in cystic fibrosis patients: 16S ribosomal DNA (rDNA) length heterogeneity PCR and 16S rDNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol , 41(8): 3548–3558 doi: 10.1128/JCM.41.8.3548-3558.2003
|
33 |
Roy P H, Tetu S G, Larouche A, Elbourne L, Tremblay S, Ren Q, Dodson R, Harkins D, Shay R, Watkins K, Mahamoud Y, Paulsen I T (2010). Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS ONE , 5(1): e8842 doi: 10.1371/journal.pone.0008842
|
34 |
Singh P K, Schaefer A L, Parsek M R, Moninger T O, Welsh M J, Greenberg E P (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature , 407(6805): 762–764 doi: 10.1038/35037627
|
35 |
Smith E E, Buckley D G, Wu Z, Saenphimmachak C, Hoffman L R, D’Argenio D A, Miller S I, Ramsey B W, Speert D P, Moskowitz S M, Burns J L, Kaul R, Olson M V, Affiliations A (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA , 103(22): 8487–8492 doi: 10.1073/pnas.0602138103
|
36 |
Spiers A J, Buckling A, Rainey P B (2000). The causes of Pseudomonas diversity. Microbiology (Reading, Engl.) , 146 (Pt 10): 2345–2350 .
|
37 |
Starkey M, Hickman J H, Ma L, Zhang N, De Long S, Hinz A, Palacios S, Manoil C, Kirisits M J, Starner T D, Wozniak D J, Harwood C S, Parsek M R (2009). Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol , 191(11): 3492–3503 doi: 10.1128/JB.00119-09
|
38 |
Stickland H G, Davenport P W, Lilley K S, Griffin J L, Welch M (2010). Mutation of nfxB causes global changes in the physiology and metabolism of Pseudomonas aeruginosa. J Proteome Res , 9(6): 2957–2967 doi: 10.1021/pr9011415
|
39 |
Stover C K, Pham X Q, Erwin A L, Mizoguchi S D, Warrener P, Hickey M J, Brinkman F S, Hufnagle W O, Kowalik D J, Lagrou M, Garber R L, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody L L, Coulter S N, Folger K R, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong G K, Wu Z, Paulsen I T, Reizer J, Saier M H, Hancock R E, Lory S, Olson M V (2000). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature , 406(6799): 959–964 doi: 10.1038/35023079
|
40 |
Stressmann F A, Rogers G B, van der Gast C J, Marsh P, Vermeer L S, Carroll M P, Hoffman L, Daniels T W V, Patel N, Forbes B, Bruce K D (2012). Long-term cultivation-independent microbial diversity analysis demonstrates that bacterial communities infecting the adult cystic fibrosis lung show stability and resilience. Thorax , 67(10): 867–873 doi: 10.1136/thoraxjnl-2011-200932
|
41 |
Tunney M M, Field T R, Moriarty T F, Patrick S, Doering G, Muhlebach M S, Wolfgang M C, Boucher R, Gilpin D F, McDowell A, Elborn J S (2008). Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med , 177(9): 995–1001 doi: 10.1164/rccm.200708-1151OC
|
42 |
van der Gast C J, Walker A W, Stressmann F A, Rogers G B, Scott P, Daniels T W, Carroll M P, Parkhill J, Bruce K D (2011). Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J , 5(5): 780–791 doi: 10.1038/ismej.2010.175
|
43 |
Williams P, Camara M (2009). Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol , 12(2): 182–191 doi: 10.1016/j.mib.2009.01.005
|
44 |
Winstanley C, Langille M G, Fothergill J L, Kukavica-Ibrulj I, Paradis-Bleau C, Sanschagrin F, Thomson N R, Winsor G L, Quail M A, Lennard N, Bignell A, Clarke L, Seeger K, Saunders D, Harris D, Parkhill J, Hancock R E, Brinkman F S, Levesque R C (2009). Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Genome Res , 19(1): 12–23 doi: 10.1101/gr.086082.108
|
45 |
Workentine M L, Sibley C D, Glezerson B, Purighalla S, Norgaard-Gron J C, Parkins M D, Rabin H R, Surette M G (2013). Phenotypic heterogeneity of Pseudomonas aeruginosa. Populations in a Cystic Fibrosis Patient. PLoS ONE , 8(4): e60225 doi: 10.1371/journal.pone.0060225
|
46 |
Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer K C, Birrer P, Bellon G, Berger J, Weiss T, Botzenhart K, Yankaskas J R, Randell S, Boucher R C, D?ring G (2002). Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest , 109: 317–325
|
47 |
Wurtzel O, Yoder-Himes D R, Han K, Dandekar A A, Edelheit S, Greenberg E P, Sorek R, Lory S (2012). The Single- Nucleotide Resolution Transcriptome of Pseudomonas aeruginosa Grown in Body Temperature. PLoS Pathog , 8(9): e1002945 doi: 10.1371/journal.ppat.1002945
|
48 |
Yang L, Jelsbak L, Marvig R L, Damki?r S, Workman C T, Rau M H, Hansen S K, Folkesson A, Johansen H K, Ciofu O, Hoiby N, Sommer M O A, Molin S (2011). Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA , 108(18): 7481–7486 doi: 10.1073/pnas.1018249108
|
49 |
Zhao J, Schloss P D, Kalikin L M, Carmody L A, Foster B K, Petrosino J F, Cavalcoli J D, VanDevanter D R, Murray S, Li J Z, Young V B, LiPuma J (2012). Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci , 109: 5809–5814
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