REVIEW

Universal soldier: Pseudomonas aeruginosa – an opportunistic generalist

  • Jeremy GROSS 1 ,
  • Ian J. PASSMORE 1 ,
  • Jade C. S. CHUNG 1 ,
  • Olena RZHEPISHEVSKA 2 ,
  • Madeleine RAMSTEDT 2 ,
  • Martin WELCH , 1
Expand
  • 1. Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, UK
  • 2. Department of Chemistry, Umeå University, Umeå 901 87, Sweden

Received date: 23 Apr 2013

Accepted date: 04 Jun 2013

Published date: 01 Aug 2013

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Jeremy GROSS , Ian J. PASSMORE , Jade C. S. CHUNG , Olena RZHEPISHEVSKA , Madeleine RAMSTEDT , Martin WELCH . Universal soldier: Pseudomonas aeruginosa – an opportunistic generalist[J]. Frontiers in Biology, 2013 , 8(4) : 387 -394 . DOI: 10.1007/s11515-013-1267-x

Acknowledgements

This review is not intended to be exhaustive and we apologize to colleagues whose work is not cited for space reasons. Work in the laboratory of MW is funded by the BBSRC and Isaac Newton Trust.
Compliance with ethics guidelines
1
Bjarnsholt T, Jensen P Ø, Jakobsen T H, Phipps R, Nielsen A K, Rybtke M T, Tolker-Nielsen T, Givskov M, Høiby N, Ciofu O (2010). Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS ONE, 5(4): e10115

DOI

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

3
Buckling A, Wills M A, Colegrave N (2003). Adaptation limits diversification of experimental bacterial populations. Science, 302(5653): 2107–2109

DOI

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

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

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

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

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

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
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

11
Foweraker J (2009). Recent advances in the microbiology of respiratory tract infection in cystic fibrosis. Br Med Bull, 89(1): 93–110

DOI

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

14
Hardin G (1960). The competitive exclusion principle. Science, 131(3409): 1292–1297

DOI

15
Häussler 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

16
Häussler S, Ziegler I, Löttel A, von Götz F, Rohde M, Wehmhöhner 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

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

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

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

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

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

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

23
MacLean R C (2005). Adaptive radiation in microbial microcosms. J Evol Biol, 18(6): 1376–1386

DOI

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

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

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

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

28
Pritt B, O’Brien L, Winn W (2007). Mucoid Pseudomonas in cystic fibrosis. Am J Clin Pathol, 128(1): 32–34

DOI

29
Rainey P B, Travisano M (1998). Adaptive radiation in a heterogeneous environment. Nature, 394(6688): 69–72

DOI

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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, Döring 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

48
Yang L, Jelsbak L, Marvig R L, Damkiær 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

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

Outlines

/