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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2013, Vol. 8 Issue (4) : 387-394    https://doi.org/10.1007/s11515-013-1267-x
REVIEW
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.

Keywords Pseudomonas aeruginosa      cystic fibrosis      evolution      adaptive radiation      antibiotic resistance      quorum sensing     
Corresponding Author(s): WELCH Martin,Email:mw240@cam.ac.uk   
Issue Date: 01 August 2013
 Cite this article:   
Jeremy GROSS,Ian J. PASSMORE,Jade C. S. CHUNG, et al. Universal soldier: Pseudomonas aeruginosa – an opportunistic generalist[J]. Front Biol, 2013, 8(4): 387-394.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-013-1267-x
https://academic.hep.com.cn/fib/EN/Y2013/V8/I4/387
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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