Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival

PLoS Pathogens

Volumn 8, Issue 5, 2012, Pages

  Ensminger, Alexander W ^a,b,c,d   Yassin, Yosuf ^e   Miron, Alexander ^e   Isberg, Ralph R ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d PUBLIC HEALTH ONTARIO   (Canada)

^e DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE;

AMOEBA (LIFE CYCLE STAGE); ANIMAL CELL; ARTICLE; AUXOTROPHY; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; BIOSYNTHESIS; CELL DIVISION; CLONAL VARIATION; CONTROLLED STUDY; FITNESS; FLAGELLUM; GENOMICS; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HOST CELL; HOST RANGE; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; POINT MUTATION; POPULATION DYNAMICS; SURVIVAL; A J MOUSE; ACANTHAMOEBA; ADAPTATION; ANIMAL; BONE MARROW CELL; CELL CULTURE; FEMALE; GENETIC SELECTION; GENETICS; HOST PATHOGEN INTERACTION; LEGIONNAIRE DISEASE; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; REPRODUCTIVE FITNESS;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; NEGIBACTERIA; PROTOZOA;

ACANTHAMOEBA; ADAPTATION, BIOLOGICAL; ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; EVOLUTION, MOLECULAR; FEMALE; GENETIC FITNESS; HOST-PATHOGEN INTERACTIONS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MICE; MICE, INBRED A; MICROBIAL VIABILITY; POINT MUTATION; SELECTION, GENETIC;

EID: 84863644574     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002731     Document Type: Article

References (94)

1. Isberg RR, O'Connor TJ, Heidtman M, (2009) The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7: 13-24.
2. Centers for Disease Control and Prevention (CDC) (2011) Legionellosis - United States, 2000-2009. MMWR Morb Mortal Wkly Rep 60: 1083-1086.
3. Joseph CA, Ricketts KD, (2010) Legionnaires disease in Europe 2007-2008. Euro Surveill 15: 19493.
4. Tijet N, Tang P, Romilowych M, Duncan C, Ng V, et al. (2010) New endemic Legionella pneumophila serogroup I clones, Ontario, Canada. Emerg Infect Dis 16: 447-454.
5. Fliermans CB, Cherry WB, Orrison LH, Thacker L, (1979) Isolation of Legionella pneumophila from nonepidemic-related aquatic habitats. Appl Environ Microbiol 37: 1239-1242.
6. Bopp CA, Sumner JW, Morris GK, Wells JG, (1981) Isolation of Legionella spp. from environmental water samples by low-pH treatment and use of a selective medium. J Clin Microbiol 13: 714-719.
7. Diederen BM, de Jong CM, Aarts I, Peeters MF, van der Zee A, (2007) Molecular evidence for the ubiquitous presence of Legionella species in Dutch tap water installations. J Water Health 5: 375-383.
8. Fields BS, (1996) The molecular ecology of legionellae. Trends Microbiol 4: 286-290.
9. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y, (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71: 20-28.
10. Rowbotham TJ, (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33: 1179-1183.
11. Burstein D, Zusman T, Degtyar E, Viner R, Segal G, et al. (2009) Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog 5: e1000508.
12. Huang L, Boyd D, Amyot WM, Hempstead AD, Luo ZQ, et al. (2011) The E Block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol 13: 227-245.
13. Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, et al. (2011) Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS One 6: e17638.
14. Clemens DL, Lee BY, Horwitz MA, (2000) Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun 68: 2671-2684.
15. Joshi AD, Sturgill-Koszycki S, Swanson MS, (2001) Evidence that Dot-dependent and-independent factors isolate the Legionella pneumophila phagosome from the endocytic network in mouse macrophages. Cell Microbiol 3: 99-114.
16. Roy CR, Berger KH, Isberg RR, (1998) Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28: 663-674.
17. O'Connor TJ, Adepoju Y, Boyd D, Isberg RR, (2011) Minimization of the Legionella pneumophila genome reveals chromosomal regions involved in host range expansion. Proc Natl Acad Sci U S A 108: 14733-14740.
18. Muder RR, Yu VL, Woo AH, (1986) Mode of transmission of Legionella pneumophila. A critical review. Arch Intern Med 146: 1607-1612.
19. McDade JE, Shepard CC, Fraser DW, Tsai TR, Redus MA, et al. (1977) Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297: 1197-1203.
20. Fraser DW, Deubner DC, Hill DL, Gilliam DK, (1979) Nonpneumonic, short-incubation-period Legionellosis (Pontiac fever) in men who cleaned a steam turbine condenser. Science 205: 690-691.
21. Gao LY, Harb OS, Abu Kwaik Y, (1997) Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant host cells, mammalian macrophages and protozoa. Infect Immun 65: 4738-4746.
22. Berger KH, Isberg RR, (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7: 7-19.
23. Brand BC, Sadosky AB, Shuman HA, (1994) The Legionella pneumophila icm locus: a set of genes required for intracellular multiplication in human macrophages. Mol Microbiol 14: 797-808.
24. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, et al. (1977) Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 297: 1189-1197.
25. Kagan JC, Stein MP, Pypaert M, Roy CR, (2004) Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 199: 1201-1211.
26. Ninio S, Roy CR, (2007) Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol 15: 372-380.
27. Ensminger AW, Isberg RR, (2009) Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr Opin Microbiol 12: 67-73.
28. Coers J, Vance RE, Fontana MF, Dietrich WF, (2007) Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell Microbiol 9: 2344-2357.
29. Dykhuizen DE, Hartl DL, (1983) Selection in chemostats. Microbiol Rev 47: 150-168.
30. Elena SF, Lenski RE, (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457-469.
31. Logsdon LK, Mecsas J, (2003) Requirement of the Yersinia pseudotuberculosis effectors YopH and YopE in colonization and persistence in intestinal and lymph tissues. Infect Immun 71: 4595-4607.
32. Ng PC, Kirkness EF, (2010) Whole genome sequencing. Methods Mol Biol 628: 215-226.
33. Samrakandi MM, Cirillo SL, Ridenour DA, Bermudez LE, Cirillo JD, (2002) Genetic and phenotypic differences between Legionella pneumophila strains. J Clin Microbiol 40: 1352-1362.
34. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, et al. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247.
35. Albert-Weissenberger C, Sahr T, Sismeiro O, Hacker J, Heuner K, et al. (2010) Control of flagellar gene regulation in Legionella pneumophila and its relation to growth phase. J Bacteriol 192: 446-455.
36. Dasgupta N, Arora SK, Ramphal R, (2000) fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 182: 357-364.
37. Luo ZQ, Isberg RR, (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci U S A 101: 841-846.
38. John EM, Miron A, Gong G, Phipps AI, Felberg A, et al. (2007) Prevalence of pathogenic BRCA1 mutation carriers in 5 US racial/ethnic groups. JAMA 298: 2869-2876.
39. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
40. Hickey EK, Cianciotto NP, (1994) Cloning and sequencing of the Legionella pneumophila fur gene. Gene 143: 117-121.
41. Chien M, Morozova I, Shi S, Sheng H, Chen J, et al. (2004) The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305: 1966-1968.
42. Kusumoto A, Kamisaka K, Yakushi T, Terashima H, Shinohara A, et al. (2006) Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus. J Biochem 139: 113-121.
43. Balaban M, Hendrixson DR, (2011) Polar flagellar biosynthesis and a regulator of flagellar number influence spatial parameters of cell division in Campylobacter jejuni. PLoS Pathog 7: e1002420.
44. Ristroph JD, Hedlund KW, Gowda S, (1981) Chemically defined medium for Legionella pneumophila growth. J Clin Microbiol 13: 115-119.
45. Scapin G, Blanchard JS, (1998) Enzymology of bacterial lysine biosynthesis. Adv Enzymol Relat Areas Mol Biol 72: 279-324.
46. Moliner C, Fournier PE, Raoult D, (2010) Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol Rev Epub ahead of print.
47. Bruggemann H, Cazalet C, Buchrieser C, (2006) Adaptation of Legionella pneumophila to the host environment: role of protein secretion, effectors and eukaryotic-like proteins. Curr Opin Microbiol 9: 86-94.
48. Travisano M, Mongold JA, Bennett AF, Lenski RE, (1995) Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267: 87-90.
49. Herring CD, Raghunathan A, Honisch C, Patel T, Applebee MK, et al. (2006) Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38: 1406-1412.
50. Almahmoud I, Kay E, Schneider D, Maurin M, (2009) Mutational paths towards increased fluoroquinolone resistance in Legionella pneumophila. J Antimicrob Chemother 64: 284-293.
51. Chou HH, Berthet J, Marx CJ, (2009) Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet 5: e1000652.
52. Quan S, Ray JC, Kwota Z, Duong T, Balazsi G, et al. (2012) Adaptive Evolution of the Lactose Utilization Network in Experimentally Evolved Populations of Escherichia coli. PLoS Genet 8: e1002444.
53. Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT, et al. (2012) Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335: 428-432.
54. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ, (1999) Different trajectories of parallel evolution during viral adaptation. Science 285: 422-424.
55. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE, (2006) Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc Natl Acad Sci U S A 103: 9107-9112.
56. Gerrish PJ, Lenski RE, (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102-103: 127-144.
57. Hegreness M, Shoresh N, Hartl D, Kishony R, (2006) An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311: 1615-1617.
58. Miller CR, Joyce P, Wichman HA, (2011) Mutational effects and population dynamics during viral adaptation challenge current models. Genetics 187: 185-202.
59. Woods RJ, Barrick JE, Cooper TF, Shrestha U, Kauth MR, et al. (2011) Second-order selection for evolvability in a large Escherichia coli population. Science 331: 1433-1436.
60. Ebert D, (1998) Experimental evolution of parasites. Science 282: 1432-1435.
61. Deardorff ER, Fitzpatrick KA, Jerzak GV, Shi PY, Kramer LD, et al. (2011) West Nile virus experimental evolution in vivo and the trade-off hypothesis. PLoS Pathog 7: e1002335.
62. Drexler K, Riede I, Montag D, Eschbach ML, Henning U, (1989) Receptor specificity of the Escherichia coli T-even type phage Ox2. Mutational alterations in host range mutants. J Mol Biol 207: 797-803.
63. Duffy S, Turner PE, Burch CL, (2006) Pleiotropic costs of niche expansion in the RNA bacteriophage phi 6. Genetics 172: 751-757.
64. Elena SF, Agudelo-Romero P, Lalic J, (2009) The evolution of viruses in multi-host fitness landscapes. Open Virol J 3: 1-6.
65. Turner PE, Elena SF, (2000) Cost of host radiation in an RNA virus. Genetics 156: 1465-1470.
66. Weaver SC, Brault AC, Kang W, Holland JJ, (1999) Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73: 4316-4326.
67. Cooper VS, Lenski RE, (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736-739.
68. Reboud X, Bell G, (1997) Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78: 507-514.
69. Ledwidge R, Blanchard JS, (1999) The dual biosynthetic capability of N-acetylornithine aminotransferase in arginine and lysine biosynthesis. Biochemistry 38: 3019-3024.
70. Lo CC, Bonner CA, Xie G, D'Souza M, Jensen RA, (2009) Cohesion group approach for evolutionary analysis of aspartokinase, an enzyme that feeds a branched network of many biochemical pathways. Microbiol Mol Biol Rev 73: 594-651.
71. Faucher SP, Mueller CA, Shuman HA, (2011) Legionella pneumophila Transcriptome during Intracellular Multiplication in Human Macrophages. Front Microbiol 2: 60.
72. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M, (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40: D109-114.
73. Sauer JD, Bachman MA, Swanson MS, (2005) The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. Proc Natl Acad Sci U S A 102: 9924-9929.
74. Hovel-Miner G, Faucher SP, Charpentier X, Shuman HA, (2010) ArgR-regulated genes are derepressed in the Legionella-containing vacuole. J Bacteriol 192: 4504-4516.
75. Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, et al. (2003) Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci U S A 100: 5455-5460.
76. La Scola B, Raoult D, (2001) Survival of Coxiella burnetii within free-living amoeba Acanthamoeba castellanii. Clin Microbiol Infect 7: 75-79.
77. Amitai Z, Bromberg M, Bernstein M, Raveh D, Keysary A, et al. (2010) A large Q fever outbreak in an urban school in central Israel. Clin Infect Dis 50: 1433-1438.
78. Mintz CS, Chen JX, Shuman HA, (1988) Isolation and characterization of auxotrophic mutants of Legionella pneumophila that fail to multiply in human monocytes. Infect Immun 56: 1449-1455.
79. Bandyopadhyay P, Liu S, Gabbai CB, Venitelli Z, Steinman HM, (2007) Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect Immun 75: 723-735.
80. Fraser DW, (1986) The Peculiarities of Legionella. Proc Am Philos Soc 130: 330-335.
81. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, et al. (2009) Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19: 2279-2287.
82. Zdziarski J, Brzuszkiewicz E, Wullt B, Liesegang H, Biran D, et al. (2010) Host imprints on bacterial genomes-rapid, divergent evolution in individual patients. PLoS Pathog 6: e1001078.
83. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, et al. (2011) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469-474.
84. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, et al. (2011) Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43: 1275-1280.
85. Yang L, Jelsbak L, Marvig RL, Damkiaer S, Workman CT, et al. (2011) Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci U S A 108: 7481-7486.
86. Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, et al. (2012) Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc Natl Acad Sci U S A 109: 3065-70.
87. Swanson MS, Isberg RR, (1996) Identification of Legionella pneumophila mutants that have aberrant intracellular fates. Infect Immun 64: 2585-2594.
88. Auerbuch V, Golenbock DT, Isberg RR, (2009) Innate immune recognition of Yersinia pseudotuberculosis type III secretion. PLoS Pathog 5: e1000686.
89. Ensminger AW, Isberg RR, (2010) E3 ubiquitin ligase activity and targeting of BAT3 by multiple Legionella pneumophila translocated substrates. Infect Immun 78: 3905-3919.
90. Zerbino DR, Birney E, (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
91. Ganguly A, Rock MJ, Prockop DJ, (1993) Conformation-sensitive gel electrophoresis for rapid detection of single-base differences in double-stranded PCR products and DNA fragments: evidence for solvent-induced bends in DNA heteroduplexes. Proc Natl Acad Sci U S A 90: 10325-10329.
92. Korkko J, Annunen S, Pihlajamaa T, Prockop DJ, Ala-Kokko L, (1998) Conformation sensitive gel electrophoresis for simple and accurate detection of mutations: comparison with denaturing gradient gel electrophoresis and nucleotide sequencing. Proc Natl Acad Sci U S A 95: 1681-1685.
93. Davies H, Dicks E, Stephens P, Cox C, Teague J, et al. (2006) High throughput DNA sequence variant detection by conformation sensitive capillary electrophoresis and automated peak comparison. Genomics 87: 427-432.
94. Velasco E, Infante M, Duran M, Perez-Cabornero L, Sanz DJ, et al. (2007) Heteroduplex analysis by capillary array electrophoresis for rapid mutation detection in large multiexon genes. Nat Protoc 2: 237-246.