Temperate phages both mediate and drive adaptive evolution in pathogen biofilms

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 29, 2016, Pages 8266-8271

  Davies, Emily V ^a   James, Chloe E ^a,b   Williams, David ^a   O'Brien, Siobhan ^c   Fothergill, Joanne L ^a   Haldenby, Sam ^a   Paterson, Steve ^a   Winstanley, Craig ^a   Brockhurst, Michael A ^c  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF SALFORD   (United Kingdom)

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Bacteriophage; Cystic fibrosis; Experimental evolution; Mobile genetic element; Pseudomonas aeruginosa

Indexed keywords

BACTERIAL CHROMOSOME; BACTERIAL GENETICS; BACTERIAL INFECTION; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BACTERIOPHAGE; BIOFILM; CONFERENCE PAPER; CONTROLLED STUDY; CYSTIC FIBROSIS; EVOLUTIONARY ADAPTATION; GENE FREQUENCY; GENE MUTATION; GENETIC VARIABILITY; HOST PARASITE INTERACTION; LUNG INFECTION; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SELECTIVE SWEEP; SPUTUM; TRANSPOSON; ADAPTATION; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MUTATION;

ADAPTATION, PHYSIOLOGICAL; BACTERIOPHAGES; BIOFILMS; BIOLOGICAL EVOLUTION; MUTATION; PSEUDOMONAS AERUGINOSA; SPUTUM;

EID: 84978849193     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1520056113     Document Type: Article

References (84)

1. Brüssow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68(3):560-602.
2. Bobay LM, Rocha EP, Touchon M (2013) The adaptation of temperate bacteriophages to their host genomes. Mol Biol Evol 30(4):737-751.
3. Bobay LM, Touchon M, Rocha EP (2014) Pervasive domestication of defective prophages by bacteria. Proc Natl Acad Sci USA 111(33):12127-12132.
4. Hockett KL, Renner T, Baltrus DA (2015) Independent co-option of a tailed bacteriophage into a killing complex in Pseudomonas. MBio 6(4):e00452.
5. Busby B, Kristensen DM, Koonin EV (2013) Contribution of phage-derived genomic islands to the virulence of facultative bacterial pathogens. Environ Microbiol 15(2):307-312.
6. Pallen MJ, Wren BW (2007) Bacterial pathogenomics. Nature 449(7164):835-842.
7. Figueroa-Bossi N, Bossi L (1999) Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33(1):167-176.
8. Figueroa-Bossi N, Uzzau S, Maloriol D, Bossi L (2001) Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol 39(2):260-271.
9. Taylor AL (1963) Bacteriophage-induced mutation in Escherichia coli. Proc Natl Acad Sci USA 50:1043-1051.
10. Rehmat S, Shapiro JA (1983) Insertion and replication of the Pseudomonas aeruginosa mutator phage D3112. Mol Gen Genet 192(3):416-423.
11. Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499(7457):219-222.
12. Letarov A, Kulikov E (2009) The bacteriophages in human- and animal body-associated microbial communities. J Appl Microbiol 107(1):1-13.
13. James CE, et al. (2015) Lytic activity by temperate phages of Pseudomonas aeruginosa in long-term cystic fibrosis chronic lung infections. ISME J 9(6):1391-1398.
14. Harrison F (2007) Microbial ecology of the cystic fibrosis lung. Microbiology 153(Pt 4):917-923.
15. Mowat E, et al. (2011) Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med 183(12):1674-1679.
16. Williams D, et al. (2015) Divergent, coexisting Pseudomonas aeruginosa lineages in chronic cystic fibrosis lung infections. Am J Respir Crit Care Med 191(7):775-785.
17. Jorth P, et al. (2015) Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe 18(3):307-319.
18. Folkesson A, et al. (2012) Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: An evolutionary perspective. Nat Rev Microbiol 10(12):841-851.
19. Diaz Caballero J, et al. (2015) Selective sweeps and parallel pathoadaptation drive Pseudomonas aeruginosa evolution in the cystic fibrosis lung. MBio 6(5):e00981-e15.
20. Winstanley C, O'Brien S, Brockhurst MA (2016) Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 24(5):327-337.
21. Fothergill JL, et al. (2011) Effect of antibiotic treatment on bacteriophage production by a cystic fibrosis epidemic strain of Pseudomonas aeruginosa. Antimicrob Agents Chemother 55(1):426-428.
22. Tejedor C, Foulds J, Zasloff M (1982) Bacteriophages in sputum of patients with bronchopulmonary Pseudomonas infections. Infect Immun 36(1):440-441.
23. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW (2011) Pseudomonas genomes: Diverse and adaptable. FEMS Microbiol Rev 35(4):652-680.
24. Miller RV, Rubero VJ (1984) Mucoid conversion by phages of Pseudomonas aeruginosa strains from patients with cystic fibrosis. J Clin Microbiol 19(5):717-719.
25. Martin DR (1973) Mucoid variation in Pseudomonas aeruginosa induced by the action of phage. J Med Microbiol 6(1):111-118.
26. Sriramulu DD, Lünsdorf H, Lam JS, Römling U (2005) Microcolony formation: A novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J Med Microbiol 54(7):667-676.
27. Winstanley C, et al. (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.
28. Fothergill JL, Walshaw MJ, Winstanley C (2012) Transmissible strains of Pseudomonas aeruginosa in cystic fibrosis lung infections. Eur Respir J 40(1):227-238.
29. Burns N, James CE, Harrison E (2015) Polylysogeny magnifies competitiveness of a bacterial pathogen in vivo. Evol Appl 8(4):346-351.
30. Lemieux AA, et al. (2016) Genes required for free phage production are essential for Pseudomonas aeruginosa chronic lung infections. J Infect Dis 213(3):395-402.
31. Davies EVJ, et al. (April 12, 2016) Temperate phages enhance pathogen fitness in chronic lung infection. ISME J, doi:10.1038/ismej.2016.51.
32. Brown SP, Le Chat L, De Paepe M, Taddei F (2006) Ecology of microbial invasions: Amplification allows virus carriers to invade more rapidly when rare. Curr Biol 16(20):2048-2052.
33. James CE, et al. (2012) Differential infection properties of three inducible prophages from an epidemic strain of Pseudomonas aeruginosa. BMC Microbiol 12:216.
34. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 9(7):797-803.
35. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28-36.
36. Grant CE, Bailey TL, Noble WS (2011) FIMO: Scanning for occurrences of a given motif. Bioinformatics 27(7):1017-1018.
37. Schuster M, Sexton DJ, Diggle SP, Greenberg EP (2013) Acyl-homoserine lactone quorum sensing: From evolution to application. Annu Rev Microbiol 67:43-63.
38. Diggle SP, Cornelis P, Williams P, Cámara M (2006) 4-quinolone signalling in Pseudomonas aeruginosa: Old molecules, new perspectives. Int J Med Microbiol 296(2-3):83-91.
39. Ghosh D, et al. (2009) Acyl-homoserine lactones can induce virus production in lysogenic bacteria: An alternative paradigm for prophage induction. Appl Environ Microbiol 75(22):7142-7152.
40. Høyland-Kroghsbo NM, Maerkedahl RB, Svenningsen SL (2013) A quorum-sensinginduced bacteriophage defense mechanism. MBio 4(1):e00362-e12.
41. Winstanley C, Fothergill JL (2009) The role of quorum sensing in chronic cystic fibrosis Pseudomonas aeruginosa infections. FEMS Microbiol Lett 290(1):1-9.
42. Jimenez PN, et al. (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76(1):46-65.
43. Roux D, et al. (2015) Fitness cost of antibiotic susceptibility during bacterial infection. Sci Transl Med 7(297):297ra114.
44. Mahenthiralingam E, Campbell ME, Speert DP (1994) Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun 62(2):596-605.
45. Chang YS, Klockgether J, Tümmler B (2007) An intragenic deletion in pilQ leads to nonpiliation of a Pseudomonas aeruginosa strain isolated from cystic fibrosis lung. FEMS Microbiol Lett 270(2):201-206.
46. Bjarnsholt T, et al.; Scandinavian Cystic Fibrosis Study Consortium (2010) Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS One 5(4):e10115.
47. Jiricny N, et al. (2014) Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis. PLoS One 9(1):e83124.
48. Breidenstein EB, de la Fuente-Núñez C, Hancock RE (2011) Pseudomonas aeruginosa: All roads lead to resistance. Trends Microbiol 19(8):419-426.
49. Alhede M, Bjarnsholt T, Givskov M, Alhede M (2014) Pseudomonas aeruginosa biofilms: Mechanisms of immune evasion. Adv Appl Microbiol 86:1-40.
50. Bell G (2008) Selection: The Mechanism of Evolution (Oxford Univ Press, New York).
51. Brockhurst MA (2015) Experimental evolution can unravel the complex causes of natural selection in clinical infections. Microbiology 161(6):1175-1179.
52. Szklarczyk D, et al. (2015) STRING v10: Protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43(Database issue):D447-D452.
53. Cock PJ, et al. (2009) Biopython: Freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25(11):1422-1423.
54. Williams D, Paterson S, Brockhurst MA, Winstanley C (2016) Refined analyses suggest that recombination is a minor source of genomic diversity in Pseudomonas aeruginosa chronic cystic fibrosis infections. Microb Genom 2(3):1-8.
55. Koch B, Jensen LE, Nybroe O (2001) A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J Microbiol Methods 45(3):187-195.
56. Taylor TB, Buckling A (2010) Competition and dispersal in Pseudomonas aeruginosa. Am Nat 176(1):83-89.
57. Kirchner S, et al. (2012) Use of artificial sputum medium to test antibiotic efficacy against Pseudomonas aeruginosa in conditions more relevant to the cystic fibrosis lung. J Vis Exp (64): e3857.
58. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10-12.
59. McKenna A, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297-1303.
60. De Pristo MA, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43(5):491-498.
61. Van der Auwera GA, et al. (2013) From FastQ data to high confidence variant calls: The Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinfor 43:11-33.
62. Bailey TL, et al. (2009) MEME SUITE: Tools for motif discovery and searching. Nucl Acids Res 37(Web Server issue):W202-W208.
63. Wong A, Rodrigue N, Kassen R (2012) Genomics of adaptation during experimental evolution of the opportunistic pathogen Pseudomonas aeruginosa. PLoS Genet 8(9):e1002928.
64. Lenski RE, Rose MR, Simpson SC, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2, 000 generations. Am Nat 138(6):1315-1341.
65. Lieberman TD, et al. (2011) Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43(12):1275-1280.
66. Hachani A, et al. (2011) Type VI secretion system in Pseudomonas aeruginosa: Secretion and multimerization of VgrG proteins. J Biol Chem 286(14):12317-12327.
67. Giltner CL, Habash M, Burrows LL (2010) Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol 398(3):444-461.
68. Xiao G, He J, Rahme LG (2006) Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 152(Pt 6):1679-1686.
69. Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69(2):376-389.
70. Schuster M, Greenberg EP (2006) A network of networks: Quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296(2-3):73-81.
71. Dasgupta N, Arora SK, Ramphal R (2000) fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 182(2):357-364.
72. Hong CS, et al. (2004) The aerotaxis transducer gene aer, but not aer-2, is transcriptionally regulated by the anaerobic regulator ANR in Pseudomonas aeruginosa. J Biosci Bioeng 97(3):184-190.
73. Kumari H, et al. (2014) LTQ-XL mass spectrometry proteome analysis expands the Pseudomonas aeruginosa AmpR regulon to include cyclic di-GMP phosphodiesterases and phosphoproteins, and identifies novel open reading frames. J Proteomics 96:328-342.
74. Pryor EE, Jr, et al. (2012) The transcription factor AmrZ utilizes multiple DNA binding modes to recognize activator and repressor sequences of Pseudomonas aeruginosa virulence genes. PLoS Pathog 8(4):e1002648.
75. Irie Y, et al. (2010) Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol Microbiol 78(1):158-172.
76. Irie Y, et al. (2012) Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 109(50):20632-20636.
77. Kuchma SL, et al. (2007) BifA, a cyclic-Di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189(22):8165-8178.
78. Harvey H, Habash M, Aidoo F, Burrows LL (2009) Single-residue changes in the C-terminal disulfide-bonded loop of the Pseudomonas aeruginosa type IV pilin influence pilus assembly and twitching motility. J Bacteriol 191(21):6513-6524.
79. Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56:289-314.
80. Alm RA, Mattick JS (1996) Identification of two genes with prepilin-like leader sequences involved in type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol 178(13):3809-3817.
81. Alm RA, Mattick JS (1995) Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol Microbiol 16(3):485-496.
82. Nguyen Y, et al. (2015) Pseudomonas aeruginosa minor pilins prime type IVa pilus assembly and promote surface display of the PilY1 adhesin. J Biol Chem 290(1):601-611.
83. Doyle TB, Hawkins AC, McCarter LL (2004) The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol 186(19):6341-6350.
84. De Vos D, et al. (1993) Detection of the outer membrane lipoprotein I and its gene in fluorescent and non-fluorescent pseudomonads: Implications for taxonomy and diagnosis. J Gen Microbiol 139(9):2215-2223.