Short-sighted evolution of bacterial opportunistic pathogens with an environmental origin

Frontiers in Microbiology

Volumn 5, Issue MAY, 2014, Pages

  Martínez, José L ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Bacterial evolution; Chronic infection; Cystic fibrosis; Opportunistic pathogen; Pseudomonas aeruginosa

Indexed keywords

ANTIBIOTIC AGENT;

BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; CYSTIC FIBROSIS; ENVIRONMENTAL DISEASE; EVOLUTION; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE MUTATION; HUMAN; NONHUMAN; NOTE; OPPORTUNISTIC INFECTION; PHYLOGENETIC TREE; PLAGUE; PLASMID; PSEUDOMONAS AERUGINOSA; YERSINIA;

EID: 84904874324     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00239     Document Type: Note

References (46)

1. Achtman, M., Morelli, G., Zhu, P., Wirth, T., Diehl, I., Kusecek, B., et al. (2004). Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl. Acad. Sci. U.S.A. 101, 17837-17842. doi: 10.1073/pnas.0408026101
2. Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A., and Carniel, E. (1999). Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. U.S.A. 96, 14043-14048. doi: 10.1073/pnas.96.24.14043
3. Alonso, A., and Martinez, J. L. (1997). Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 41, 1140-1142.
4. Alonso, A., Rojo, F., and Martinez, J. L. (1999). Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ. Microbiol. 1, 421-430. doi: 10.1046/j.1462-2920.1999.00052.x
5. Ashish, A., Shaw, M., Winstanley, C., Humphreys, L., and Walshaw, M. J. (2013). Halting the spread of epidemic Pseudomonas aeruginosa in an adult cystic fibrosis centre: a prospective cohort study. JRSM Short Rep. 4:1. doi: 10.1258/shorts.2012.012018
6. Bergogne-Berezin, E., Decre, D., and Joly-Guillou, M. L. (1993). Opportunistic nosocomial multiply resistant bacterial infections-their treatment and prevention. J. Antimicrob. Chemother. 32(Suppl. A), 39-47. doi: 10.1093/jac/32.suppl_A.39
7. Bragonzi, A., Paroni, M., Nonis, A., Cramer, N., Montanari, S., Rejman, J., et al. (2009). Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am. J. Respir. Crit. Care Med. 180, 138-145. doi: 10.1164/rccm.200812-1943OC
8. Broderick, K. E., Chan, A., Balasubramanian, M., Feala, J., Reed, S. L., Panda, M., et al. (2008). Cyanide produced by human isolates of Pseudomonas aeruginosa contributes to lethality in Drosophila melanogaster. J. Infect. Dis. 197, 457-464. doi: 10.1086/525282
9. Carilla-Latorre, S., Calvo-Garrido, J., Bloomfield, G., Skelton, J., Kay, R. R., Ivens, A., et al. (2008). Dictyostelium transcriptional responses to Pseudomonas aeruginosa: common and specific effects from PAO1 and PA14 strains. BMC Microbiol. 8:109. doi: 10.1186/1471-2180-8-109
10. Chouikha, I., and Hinnebusch, B. J. (2012). Yersinia-flea interactions and the evolution of the arthropod-borne transmission route of plague. Curr. Opin. Microbiol. 15, 239-246. doi: 10.1016/j.mib.2012.02.003
11. Cosson, P., Zulianello, L., Join-Lambert, O., Faurisson, F., Gebbie, L., Benghezal, M., et al. (2002). Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J. Bacteriol. 184, 3027-3033. doi: 10.1128/JB.184.11.3027-3033.2002
12. Damkiaer, S., Yang, L., Molin, S., and Jelsbak, L. (2013). Evolutionary remodeling of global regulatory networks during long-term bacterial adaptation to human hosts. Proc. Natl. Acad. Sci. U.S.A. 110, 7766-7771. doi: 10.1073/pnas.1221466110
13. Dettman, J. R., Rodrigue, N., Aaron, S. D., and Kassen, R. (2013). Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 110, 21065-21070. doi: 10.1073/pnas.1307862110
14. Folkesson, A., Jelsbak, L., Yang, L., Johansen, H. K., Ciofu, O., Hoiby, N., et al. (2012). Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat. Rev. Microbiol. 10, 841-851. doi: 10.1038/nrmicro2907
15. Friman, V. P., Ghoul, M., Molin, S., Johansen, H. K., and Buckling, A. (2013). Pseudomonas aeruginosa adaptation to lungs of cystic fibrosis patients leads to lowered resistance to phage and protist enemies. PLoS ONE 8:e75380. doi: 10.1371/journal.pone.0075380
16. Gal-Mor, O., and Finlay, B. B. (2006). Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell. Microbiol. 8, 1707-1719. doi: 10.1111/j.1462-5822.2006.00794.x
17. Groisman, E. A., and Ochman, H. (1996). Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87, 791-794. doi: 10.1016/S0092-8674(00)81985-6
18. Jelsbak, L., Johansen, H. K., Frost, A. L., Thogersen, R., Thomsen, L. E., Ciofu, O., et al. (2007). Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect. Immun. 75, 2214-2224. doi: 10.1128/IAI.01282-06
19. Jiricny, N., Molin, S., Foster, K., Diggle, S. P., Scanlan, P. D., Ghoul, M., et al. (2014). Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis. PLoS ONE 9:e83124. doi: 10.1371/journal.pone.0083124
20. Kidd, T. J., Ritchie, S. R., Ramsay, K. A., Grimwood, K., Bell, S. C., and Rainey, P. B. (2012). Pseudomonas aeruginosa exhibits frequent recombination, but only a limited association between genotype and ecological setting. PLoS ONE 7:e44199. doi: 10.1371/journal.pone.0044199
21. Koch, C., and Hoiby, N. (1993). Pathogenesis of cystic fibrosis. Lancet 341, 1065-1069. doi: 10.1016/0140-6736(93)92422-P
22. Levin, B. R., and Bull, J. J. (1994). Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2, 76-81. doi: 10.1016/0966-842X(94)90538-X
23. Mahajan-Miklos, S., Rahme, L. G., and Ausubel, F. M. (2000). Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Mol. Microbiol. 37, 981-988. doi: 10.1046/j.1365-2958.2000.02056.x
24. Mahajan-Miklos, S., Tan, M. W., Rahme, L. G., and Ausubel, F. M. (1999). Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 47-56. doi: 10.1016/S0092-8674(00)80958-7
25. Martinez, J. L. (2013). Bacterial pathogens: from natural ecosystems to human hosts. Environ. Microbiol. 15, 325-333. doi: 10.1111/j.1462-2920.2012.02837.x
26. Martinez, J. L., and Baquero, F. (2002). Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin. Microbiol. Rev. 15, 647-679. doi: 10.1128/CMR.15.4.647-679.2002
27. Martinez-Solano, L., Macia, M. D., Fajardo, A., Oliver, A., and Martinez, J. L. (2008). Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin. Infect. Dis. 47, 1526-1533. doi: 10.1086/593186
28. McHenry, H. M. (1994). Tempo and mode in human evolution. Proc. Natl. Acad. Sci. U.S.A. 91, 6780-6786. doi: 10.1073/pnas.91.15.6780
29. Mena, A., Smith, E. E., Burns, J. L., Speert, D. P., Moskowitz, S. M., Perez, J. L., et al. (2008). Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J. Bacteriol. 190, 7910-7917. doi: 10.1128/JB.01147-08
30. Morales, G., Wiehlmann, L., Gudowius, P., van Delden, C., Tummler, B., Martinez, J. L., et al. (2004). Structure of Pseudomonas aeruginosa populations analyzed by single nucleotide polymorphism and pulsed-field gel electrophoresis genotyping. J. Bacteriol. 186, 4228-4237. doi: 10.1128/JB.186.13.4228-4237.2004
31. Morschhauser, J., Kohler, G., Ziebuhr, W., Blum-Oehler, G., Dobrindt, U., and Hacker, J. (2000). Evolution of microbial pathogens. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 695-704. doi: 10.1098/rstb.2000.0609
32. Navas, A., Cobas, G., Talavera, M., Ayala, J. A., Lopez, J. A., and Martinez, J. L. (2007). Experimental validation of Haldane's hypothesis on the role of infection as an evolutionary force for Metazoans. Proc. Natl. Acad. Sci. U.S.A. 104, 13728-13731. doi: 10.1073/pnas.0704497104
33. Ojeniyi, B., Frederiksen, B., and Hoiby, N. (2000). Pseudomonas aeruginosa cross-infection among patients with cystic fibrosis during a winter camp. Pediatr. Pulmonol. 29, 177-181. doi: 10.1002/(SICI)1099-0496(200003)29:3%3C177::AID-PPUL4%3E3.0.CO;2-U
34. Oliver, A., Canton, R., Campo, P., Baquero, F., and Blazquez, J. (2000). High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288, 1251-1254. doi: 10.1126/science.288.5469.1251
35. Perez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M., Michelena, J. M., et al. (2006). A small microbial genome: the end of a long symbiotic relationship? Science 314, 312-313. doi: 10.1126/science.1130441
36. Rahme, L. G., Stevens, E. J., Wolfort, S. F., Shao, J., Tompkins, R. G., and Ausubel, F. M. (1995). Common virulence factors for bacterial pathogenicity in plants and animals. Science 268, 1899-1902. doi: 10.1126/science.7604262
37. Rau, M. H., Hansen, S. K., Johansen, H. K., Thomsen, L. E., Workman, C. T., Nielsen, K. F., et al. (2010). Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ. Microbiol. 12, 1643-1658. doi: 10.1111/j.1462-2920.2010.02211.x
38. Sanchez, M. B., Hernandez, A., and Martinez, J. L. (2009). Stenotrophomonas maltophilia drug resistance. Future Microbiol. 4, 655-660. doi: 10.2217/fmb.09.45
39. Sokurenko, E. V., Gomulkiewicz, R., and Dykhuizen, D. E. (2006). Source-sink dynamics of virulence evolution. Nat. Rev. Microbiol. 4, 548-555. doi: 10.1038/nrmicro1446
40. Tan, M. W., Mahajan-Miklos, S., and Ausubel, F. M. (1999). Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 96, 715-720. doi: 10.1073/pnas.96.2.715
41. Wiehlmann, L., Wagner, G., Cramer, N., Siebert, B., Gudowius, P., Morales, G., et al. (2007). Population structure of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 104, 8101-8106. doi: 10.1073/pnas.0609213104
42. Winstanley, C., Langille, M. G., Fothergill, J. L., Kukavica-Ibrulj, I., Paradis-Bleau, C., Sanschagrin, F., 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, 12-23. doi: 10.1101/gr.086082.108
43. Wood, B. (1992). Origin and evolution of the genus Homo. Nature 355, 783-790. doi: 10.1038/355783a0
44. Wren, B. W. (2003). The yersiniae-a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol. 1, 55-64. doi: 10.1038/nrmicro730
45. Yang, L., Jelsbak, L., Marvig, R. L., Damkiar, S., Workman, C. T., Rau, M. H., et al. (2011). Evolutionary dynamics of bacteria in a human host environment. Proc. Natl. Acad. Sci. U.S.A. 108, 7481-7486. doi: 10.1073/pnas.1018249108
46. Zhou, D., and Yang, R. (2009). Molecular Darwinian evolution of virulence in Yersinia pestis. Infect. Immun. 77, 2242-2250. doi: 10.1128/IAI.01477-08