Macrophage adaptation leads to parallel evolution of genetically diverse Escherichia coli small-colony variants with increased fitness in vivo and antibiotic collateral sensitivity

Evolutionary Applications

Volumn 9, Issue 8, 2016, Pages 994-1004

  Ramiro, Ricardo S ^a   Costa, Henrique ^a   Gordo, Isabel ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

antibiotic resistance; collateral sensitivity; experimental evolution; macrophages; mouse gut colonization; small colony variants; whole genome sequencing

Indexed keywords

EID: 84977136789     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12397     Document Type: Article

References (77)

1. Al Mamun, A. A. M., Lombardo, M.-J., Shee, C., Lisewski, A. M., Gonzalez, C., Lin, D., … Nehring, R. B. (2012). Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science, 338, 1344–1348.
2. Alefounder, P. R., Abell, C., & Battersby, A. R. (1988). The sequence of hemC, hemD and two additional E. coli genes. Nucleic Acids Research, 16, 9871.
3. Azevedo, M., Sousa, A., Moura de Sousa, J., Thompson, J. A., Proença, J. T., & Gordo, I. (2016). Trade-offs of Escherichia coli adaptation to an intracellular lifestyle in macrophages. PLoS One, 11, e0146123.
4. Bailey, S. F., & Bataillon, T. (2016). Can the experimental evolution programme help us elucidate the genetic basis of adaptation in nature? Molecular Ecology, 25, 203–218.
5. Barroso-Batista, J., Demengeot, J., & Gordo, I. (2015). Adaptive immunity increases the pace and predictability of evolutionary change in commensal gut bacteria. Nature Communications, 6, 8945.
6. Barroso-Batista, J., Sousa, A., Lourenço, M., Bergman, M. L., Sobral, D., Demengeot, J., … Gordo, I. (2014). The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genetics, 10, e1004182.
7. Baym, M., Stone, L. K., & Kishony, R. (2016). Multidrug evolutionary strategies to reverse antibiotic resistance. Science, 351, aad3292.
8. Cano, D. A., Pucciarelli, M. G., Martínez-Moya, M., Casadesús, J., & García-del Portillo, F. (2003). Selection of small-colony variants of Salmonella enterica serovar typhimurium in nonphagocytic eucaryotic cells. Infection and Immunity, 71, 3690–3698.
9. Carryn, S., Van Bambeke, F., Mingeot-Leclercq, M.-P., & Tulkens, P. M. (2002). Comparative intracellular (THP-1 macrophage) and extracellular activities of beta-lactams, azithromycin, gentamicin, and fluoroquinolones against Listeria monocytogenes at clinically relevant concentrations. Antimicrobial Agents and Chemotherapy, 46, 2095–2103.
10. Conway, T., Krogfelt, K., & Cohen, P. (2004). The life of commensal Escherichia coli in the mammalian intestine. EcoSal Plus, 1, 1–15.
11. Cooper, V. S., Staples, R. K., Traverse, C. C., & Ellis, C. N. (2014). Parallel evolution of small colony variants in Burkholderia cenocepacia biofilms. Genomics, 104, 447–452.
12. Dean, M. A., Olsen, R. J., Long, S. W., Rosato, A. E., & Musser, J. M. (2014). Identification of point mutations in clinical Staphylococcus aureus strains that produce small-colony variants auxotrophic for menadione. Infection and Immunity, 82, 1600–1605.
13. Deatherage, D. E., & Barrick, J. E. (2014). Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods in Molecular Biology, 1151, 165–188.
14. Dettman, J. R., Rodrigue, N., Melnyk, A. H., Wong, A., Bailey, S. F., & Kassen, R. (2012). Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Molecular Ecology, 21, 2058–2077.
15. Durão, P., Güleresi, D., Proença, J., & Gordo, I. (in press). Enhanced survival of Rifampicin and Streptomycin double resistant E. coli inside macrophages. Antimicrobial Agents and Chemotherapy.
16. Dykhuizen, D. E. (1990). Experimental studies of natural selection in bacteria. Annual Review of Ecology and Systematics, 21, 373–398.
17. Edwards, M. D., Black, S., Rasmussen, T., Rasmussen, A., Stokes, N. R., Stephen, T. L., … Booth, I. R. (2012). Characterization of three novel mechanosensitive channel activities in Escherichia coli. Channels Austin Tex, 6, 272–281.
18. von Eiff, C., Bettin, D., Proctor, R. A., Rolauffs, B., Lindner, N., Winkelmann, W., & Peters, G. (1997). Recovery of small colony variants of Streptococcus aureus following gentamicin bead placement for osteomyelitis. Clinical Infectious Diseases, 25, 1250–1251.
19. Elena, S. F., & Lenski, R. E. (2003). Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation. Nature Reviews Genetics, 4, 457–469.
20. Ensminger, A. W., Yassin, Y., Miron, A., & Isberg, R. R. (2012). Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival. PLoS Pathogens, 8, e1002731.
21. Friesen, M. L., Saxer, G., Travisano, M., & Doebeli, M. (2004). Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution, 58, 245–260.
22. Gonzales, P. R., Pesesky, M. W., Bouley, R., Ballard, A., Biddy, B. A., Suckow, M. A., … Dantas, G. (2015). Synergistic, collaterally sensitive β-lactam combinations suppress resistance in MRSA. Nature Chemical Biology, 11, 855–861.
23. Green, G. N., Kranz, R. G., Lorence, R. M., & Gennis, R. B. (1984). Identification of subunit I as the cytochrome b558 component of the cytochrome d terminal oxidase complex of Escherichia coli. Journal of Biological Chemistry, 259, 7994–7997.
24. Gupta, S., Mat-Jan, F., Latifi, M., & Clark, D. P. (2000). Acetaldehyde dehydrogenase activity of the AdhE protein of Escherichia coli is inhibited by intermediates in ubiquinone synthesis. FEMS Microbiology Letters, 182, 51–55.
25. Häussler, S., Tümmler, B., Weißbrodt, H., Rohde, M., & Steinmetz, I. (1999). Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clinical Infectious Diseases, 29, 621–625.
26. Herron, M. D., & Doebeli, M. (2013). Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biology, 11, e1001490.
27. Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2008). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4, 44–57.
28. Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009). Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37, 1–13.
29. Ilag, L. L., Jahn, D., Eggertsson, G., & Söll, D. (1991). The Escherichia coli hemL gene encodes glutamate 1-semialdehyde aminotransferase. Journal of Bacteriology, 173, 3408–3413.
30. Imamovic, L., & Sommer, M. O. A. (2013). Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Science Translational Medicine, 5, 204ra132–204ra132.
31. Joyce, A. R., Reed, J. L., White, A., Edwards, R., Osterman, A., Baba, T., … Agarwalla, S. (2006). Experimental and computational assessment of conditionally essential genes in Escherichia coli. Journal of Bacteriology, 188, 8259–8271.
32. Kastbjerg, V. G., Hein-Kristensen, L., & Gram, L. (2014). Triclosan induced aminoglycoside-tolerant Listeria monocytogenes isolates can appear as small-colony variants. Antimicrobial Agents Chemotherapy, doi: 10.1128/AAC.02266-13.
33. Koli, P., Sudan, S., Fitzgerald, D., Adhya, S., & Kar, S. (2011). Conversion of commensal Escherichia coli K-12 to an invasive form via expression of a mutant histone-like protein. mBio, 2, e00182–11.
34. Lázár, V., Singh, G. P., Spohn, R., Nagy, I., Horváth, B., Hrtyan, M., … Pósfai, G. (2013). Bacterial evolution of antibiotic hypersensitivity. Molecular Systems Biology, 9, 700.
35. Lee, S. M., Wyse, A., Lesher, A., Everett, M. L., Lou, L., Holzknecht, Z. E., … Parker, W. (2010). Adaptation in a mouse colony monoassociated with Escherichia coli K-12 for more than 1,000 days. Applied and Environment Microbiology, 76, 4655–4663.
36. Limoli, D. H., Rockel, A. B., Host, K. M., Jha, A., Kopp, B. T., Hollis, T., & Wozniak, D. J. (2014). Cationic antimicrobial peptides promote microbial mutagenesis and pathoadaptation in chronic infections. PLoS Pathogens, 10, e1004083.
37. McDonald, M. J., Gehrig, S. M., Meintjes, P. L., Zhang, X.-X., & Rainey, P. B. (2009). Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics, 183, 1041–1053.
38. Miskinyte, M., & Gordo, I. (2013). Increased survival of antibiotic-resistant Escherichia coli inside macrophages. Antimicrobial Agents and Chemotherapy, 57, 189–195.
39. Miskinyte, M., & Gordo, I. (2014). Fitness measurements of evolved Esherichia coli. Bio-Protocol, 4, e1228.
40. Miskinyte, M., Sousa, A., Ramiro, R. S., de Sousa, J. A. M., Kotlinowski, J., Caramalho, I., … Gordo, I. (2013). The genetic basis of Escherichia coli pathoadaptation to macrophages. PLoS Pathogens, 9, e1003802.
41. Musher, D. M., Baughn, R. E., Templeton, G. B., & Minuth, J. N. (1977). Emergence of variant forms of Staphylococcus aureus after exposure to gentamicin and infectivity of the variants in experimental animals. Journal of Infectious Diseases, 136, 360–369.
42. Nguyen, H. A., Denis, O., Vergison, A., Theunis, A., Tulkens, P. M., Struelens, M. J., & Van Bambeke, F. (2009). Intracellular activity of antibiotics in a model of human THP-1 macrophages infected by a Staphylococcus aureus small-colony variant strain isolated from a cystic fibrosis patient: Pharmacodynamic evaluation and comparison with isogenic normal-phenotype and revertant strains. Antimicrobial Agents and Chemotherapy, 53, 1434–1442.
43. Ote, T., Hashimoto, M., Ikeuchi, Y., Su'etsugu, M., Suzuki, T., Katayama, T., & Kato, J. I. (2006). Involvement of the Escherichia coli folate-binding protein YgfZ in RNA modification and regulation of chromosomal replication initiation. Molecular Microbiology, 59, 265–275.
44. Oz, T., Guvenek, A., Yildiz, S., Karaboga, E., Tamer, Y. T., Mumcuyan, N., … Toprak, E. (2014). Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution. Molecular Biology and Evolution, 31, 2387–2401.
45. Penterman, J., Nguyen, D., Anderson, E., Staudinger, B. J., Greenberg, E. P., Lam, J. S., & Singh, P. K. (2014). Rapid evolution of culture-impaired bacteria during adaptation to biofilm growth. Cell Reports, 6, 293–300.
46. Pranting, M., & Andersson, D. I. (2010). Mechanisms and physiological effects of protamine resistance in Salmonella enterica serovar Typhimurium LT2. Journal of Antimicrobial Chemotherapy, 65, 876–887.
47. Proctor, R. A., van Langevelde, P., Kristjansson, M., Maslow, J. N., & Arbeit, R. D. (1995). Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clinical Infectious Diseases, 20, 95–102.
48. Proctor, R. A., Von Eiff, C., Kahl, B. C., Becker, K., McNamara, P., Herrmann, M., & Peters, G. (2006). Small colony variants: A pathogenic form of bacteria that facilitates persistent and recurrent infections. Nature Reviews Microbiology, 4, 295–305.
49. Rainey, P. B., & Travisano, M. (1998). Adaptive radiation in a heterogeneous environment. Nature, 394, 69–72.
50. Roemhild, R., Barbosa, C., Beardmore, R. E., Jansen, G., & Schulenburg, H. (2015). Temporal variation in antibiotic environments slows down resistance evolution in pathogenic Pseudomonas aeruginosa. Evolutionary Applications, 8, 945–955.
51. Roggenkamp, A., Sing, A., Hornef, M., Brunner, U., Autenrieth, I. B., & Heesemann, J. (1998). Chronic prosthetic hip infection caused by a small-colony variant of Escherichia coli. Journal of Clinical Microbiology, 36, 2530–2534.
52. Rozen, N., & Lenski, N. (2000). Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. The American Naturalist, 155, 24–35.
53. Rusthoven, J. J., Davies, T. A., & Lerner, S. A. (1979). Clinical isolation and characterization of aminoglycoside-resistant small colony variants of Enterobacter aerogenes. American Journal of Medicine, 67, 702–706.
54. Schellhorn, H. E. (1995). Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiology Letters, 131, 113–119.
55. Smith, E. E., Buckley, D. G., Wu, Z., Saenphimmachak, C., Hoffman, L. R., D'Argenio, D. A., … Olson, M. V. (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proceedings of the National Academy of Sciences of the United States of America, 103, 8487–8492.
56. Sniegowski, P. D., & Gerrish, P. J. (2010). Beneficial mutations and the dynamics of adaptation in asexual populations. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365, 1255–1263.
57. Stroobant, P., Young, I. G., & Gibson, F. (1972). Mutants of Escherichia coli K-12 blocked in the final reaction of ubiquinone biosynthesis: Characterization and genetic analysis. Journal of Bacteriology, 109, 134–139.
58. Suzuki, S., Horinouchi, T., & Furusawa, C. (2014). Prediction of antibiotic resistance by gene expression profiles. Nature Communications, 5, 1–12.
59. Szybalski, W., & Bryson, V. (1952). Genetic studies on microbial cross resistance to toxic agents I. Cross resistance of Escherichia coli to fifteen antibiotics. Journal of Bacteriology, 64, 489–499.
60. Traverse, C. C., Mayo-Smith, L. M., Poltak, S. R., & Cooper, V. S. (2013). Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proceedings of the National Academy of Sciences of the United States of America, 110, E250–259.
61. Trindade, S., Sousa, A., & Gordo, I. (2012). Antibiotic resistance and stress in the light of fisher's model. Evolution, 66, 3815–3824.
62. Trindade, S., Sousa, A., Xavier, K.B., Dionisio, F., Ferreira, M.G., & Gordo, I. (2009). Positive epistasis drives the acquisition of multidrug resistance. PLoS Genetics, 5, e1000578.
63. Trülzsch, K., Hoffmann, H., Keller, C., Schubert, S., Bader, L., Heesemann, J., & Roggenkamp, A. (2003). Highly resistant metabolically deficient dwarf mutant of Escherichia coli is the cause of a chronic urinary tract infection. Journal of Clinical Microbiology, 41, 5689–5694.
64. Tuchscherr, L., Medina, E., Hussain, M., Völker, W., Heitmann, V., Niemann, S., … Löffler, B. (2011). Staphylococcus aureus phenotype switching: An effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Molecular Medicine, 3, 129–141.
65. Vázquez, C. L., Lerner, T. R., Kasmapour, B., Pei, G., Gronow, A., Bianco, M. V., … Gutierrez, M. G. (2014). Experimental selection of long-term intracellular mycobacteria. Cellular Microbiology, 16, 1425–1440.
66. Vesga, O., Groeschel, M. C., Otten, M. F., Brar, D. W., Vann, J. M., & Proctor, R. A. (1996). Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. Journal of Infectious Diseases, 173, 739–742.
67. Waller, J. C., Alvarez, S., Naponelli, V., Lara-Nuñez, A., Blaby, I. K., Da Silva, V., … Hanson, A. D. (2010). A role for tetrahydrofolates in the metabolism of iron-sulfur clusters in all domains of life. Proceedings of the National Academy of Sciences of the United States of America, 107, 10412–10417.
68. Wartenberg, A., Linde, J., Martin, R., Schreiner, M., Horn, F., Jacobsen, I. D., … Hube, B. (2014). Microevolution of Candida albicans in macrophages restores filamentation in a nonfilamentous mutant. PLoS Genetics, 10, e1004824.
69. Way, S. S., Sallustio, S., Magliozzo, R. S., & Goldberg, M. B. (1999). Impact of either elevated or decreased levels of cytochrome bd expression on Shigella flexneri virulence. Journal of Bacteriology, 181, 1229–1237.
70. Wei, Q., Tarighi, S., Dötsch, A., Häussler, S., Müsken, M., Wright, V. J., … Cornelis, P. (2011). Phenotypic and genome-wide analysis of an antibiotic-resistant small colony variant (SCV) of Pseudomonas aeruginosa. PLoS One, 6, e29276.
71. Weidner, U., Geier, S., Ptock, A., Friedrich, T., Leif, H., & Weiss, H. (1993). The gene locus of the proton-translocating NADH: Ubiquinone oxidoreductase in Escherichia coli: Organization of the 14 genes and relationship between the derived proteins and subunits of mitochondrial complex I. Journal of Molecular Biology, 233, 109–122.
72. Wilson, K. (2001) Preparation of genomic DNA from bacteria. Current Protocols in Molecular Biology (pp. 2–4). NY: John Wiley & Sons, Inc.
73. Wynn, T. A., Chawla, A., & Pollard, J. W. (2013). Macrophage biology in development, homeostasis and disease. Nature, 496, 445–455.
74. Yegian, D., Gallo, G., & Toll, M. W. (1959). Kanamycin resistant staphylococcus mutant requiring heme for growth. Journal of Bacteriology, 78, 10–12.
75. Yoshimoto, T., Murayama, N., Honda, T., Tone, H., & Tsuru, D. (1988). Cloning and expression of Aminopeptidase P gene from Escherichia coli HB101 and characterization of expressed enzyme. Journal of Biochemistry (Tokyo), 104, 93–97.
76. Young, I. G., Stroobant, P., Macdonald, C. G., & Gibson, F. (1973). Pathway for ubiquinone biosynthesis in Escherichia coli K-12: Gene-enzyme relationships and intermediates. Journal of Bacteriology, 114, 42–52.
77. Young, I. G., & Wallace, B. J. (1976). Mutations affecting the reduced nicotinamide adenine dinucleotide dehydrogenase complex of Escherichia coli. Biochimica et Biophysica Acta, 449, 376–385.