Isolated cell behavior drives the evolution of antibiotic resistance

Molecular Systems Biology

Volumn 11, Issue 7, 2015, Pages

  Artemova, Tatiana ^a   Gerardin, Ylaine ^b   Dudley, Carmel ^a   Vega, Nicole M ^a   Gore, Jeff ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

antibiotic resistance; beta lactamase; cooperative growth; evolution

Indexed keywords

CEFOTAXIME; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; CELL DENSITY; CELL FUNCTION; CELL ISOLATION; CONCENTRATION (PARAMETERS); ESCHERICHIA COLI; IN VIVO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; BIOLOGICAL MODEL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MICROBIAL SENSITIVITY TEST; MOLECULAR EVOLUTION; PROCEDURES; REPRODUCTIVE FITNESS;

BACTERIA (MICROORGANISMS);

ANTI-BACTERIAL AGENTS; CEFOTAXIME; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENETIC FITNESS; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; SINGLE-CELL ANALYSIS;

EID: 84938070426     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20145888     Document Type: Article

References (54)

1. Ackermann M, Stecher B, Freed NE, Songhet P, Hardt W-D, Doebeli M, (2008) Self-destructive cooperation mediated by phenotypic noise. Nature 454: 987-990
2. Andrews JM, (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48: 5-16
3. Bennett PM, (2008) Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153: S347-S357
4. Björkman J, Nagaev I, Berg OG, Hughes D, Andersson DI, (2000) Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479-1482
5. Bonomo RA, Tolmasky M, (2007) Enzyme-mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition. Washington, DC: ASM Press
6. Brook I, (1989) Inoculum effect. Rev Infect Dis 11: 361
7. Brown JE, Del Bene VE, Collins CD, (1981) In vitro activity of N-formimidoyl thienamycin, moxalactam, and other new beta-lactam agents against Bacteroides fragilis: contribution of beta-lactamase to resistance. Antimicrob Agents Chemother 19: 248-252
8. Bush K, Jacoby GA, Medeiros AA, (1995) A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrob Agents Chemother 39: 1211
9. Chadwick P, (1966) Field trial of a microcolony method for testing the antibiotic sensitivity of bacteria. Can Med Assoc J 95: 852
10. Choi J, Jung Y-G, Kim J, Kim S, Jung Y, Na H, Kwon S, (2013) Rapid antibiotic susceptibility testing by tracking single cell growth in a microfluidic agarose channel system. Lab Chip 13: 280-287
11. Chung HS, Yao Z, Goehring NW, Kishony R, Beckwith J, Kahne D, (2009) Rapid β-lactam-induced lysis requires successful assembly of the cell division machinery. Proc Natl Acad Sci 106: 21872-21877
12. Clark DR, Alton TM, Bajorek A, Holden P, Dugatkin LA, Atlas RM, Perlin MH, (2009) Evolution of altruists and cheaters in near-isogenic populations of Escherichia coli. Front Biosci 14: 4815
13. Clinical and Laboratory Standards Institute (2009) Performance standards for antimicrobial susceptibility testing of anaerobic bacteria: informational supplement. Wayne, PA: Clinical and Laboratory Standards Institute
14. Clinical and Laboratory Standards Institute (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Approved Standard-Ninth Edition. CLSI document M07-A9. Wayne, PA: Clinical and Laboratory Standards Institute
15. Cowen LE, Kohn LM, Anderson JB, (2001) Divergence in fitness and evolution of drug resistance in experimental populations of Candida albicans. J Bacteriol 183: 2971-2978
16. Damore JA, Gore J, (2012) Understanding microbial cooperation. J Theor Biol 299: 31-41
17. Dugatkin LA, Perlin M, Lucas JS, Atlas R, (2005) Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm. Proc R Soc B Biol Sci 272: 79-83
18. Ewbank JJ, Zugasti O, (2011) C. elegans: model host and tool for antimicrobial drug discovery. Dis Model Mech 4: 300-304
19. Goldstein EJ, Citron DM, Cherubin CE, (1991) Comparison of the inoculum effects of members of the family Enterobacteriaceae on cefoxitin and other cephalosporins, beta-lactamase inhibitor combinations, and the penicillin-derived components of these combinations. Antimicrob Agents Chemother 35: 560-566
20. Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D, Andersson DI, (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7: e1002158
21. Hall BG, (2002) Predicting evolution by in vitro evolution requires determining evolutionary pathways. Antimicrob Agents Chemother 46: 3035-3038
22. Hermsen R, Deris JB, Hwa T, (2012) On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient. Proc Natl Acad Sci 109: 10775-10780
23. Jacoby GA, (2006) β-lactamase nomenclature. Antimicrob Agents Chemother 50: 1123-1129
24. Johnson PJT, Levin BR, (2013) Pharmacodynamics, population dynamics, and the evolution of persistence in Staphylococcus aureus. PLoS Genet 9: e1003123
25. Leclercq R, (2002) Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clin Infect Dis 34: 482-492
26. Lee HH, Molla MN, Cantor CR, Collins JJ, (2010) Bacterial charity work leads to population-wide resistance. Nature 467: 82-85
27. Madigan MT, Martinko JM, Dunlap PV, Clark DP, (2009) Brock Biology of Microorganisms. San Francisco: Pearson Benjamin Cummings
28. Martínez JL, (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321: 365-367
29. Meredith HR, Srimani JK, Lee AJ, Lopatkin AJ, You L, (2015) Collective antibiotic tolerance: mechanisms, dynamics and intervention. Nat Chem Biol 11: 182-188
30. Mohan R, Mukherjee A, Sevgen SE, Sanpitakseree C, Lee J, Schroeder CM, Kenis PJA, (2013) A multiplexed microfluidic platform for rapid antibiotic susceptibility testing. Biosens Bioelectron 49: 118-125
31. Moy TI, Ball AR, Anklesaria Z, Casadei G, Lewis K, Ausubel FM, (2006) Identification of novel antimicrobials using a live-animal infection model. Proc Natl Acad Sci 103: 10414-10419
32. Negri M-C, Lipsitch M, Blázquez J, Levin BR, Baquero F, (2000) Concentration-dependent selection of small phenotypic differences in TEM β-lactamase-mediated antibiotic resistance. Antimicrob Agents Chemother 44: 2485-2491
33. Nikaido H, Normark S, (1987) Sensitivity of Escherichia coli to various beta-lactams is determined by the interplay of outer membrane permeability and degradation by periplasmic beta-lactamases: a quantitative predictive treatment. Mol Microbiol 1: 29-36
34. Normark BH, Normark S, (2002) Evolution and spread of antibiotic resistance. J Intern Med 252: 91-106
35. Nowak MA, (2006) Five rules for the evolution of cooperation. Science 314: 1560-1563
36. Paulander W, Pennhag A, Andersson DI, Maisnier-Patin S, (2007) Caenorhabditis elegans as a model to determine fitness of antibiotic-resistant Salmonella enterica serovar typhimurium. Antimicrob Agents Chemother 51: 766-769
37. Philippon A, Labia R, Jacoby G, (1989) Extended-spectrum beta-lactamases. Antimicrob Agents Chemother 33: 1131
38. Shaw KJ, Rather PN, Hare RS, Miller GH, (1993) Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol Rev 57: 138-163
39. Soong J, Soni N, (2012) Sepsis: recognition and treatment. Clin Med 12: 276-280
40. Stemmer WPW, (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370: 389-391
41. Stiernagle T, (2006) Maintenance of C. elegans. In WormBook, ed. The C. elegans Research Community, WormBook
42. Sykes RB, Matthew M, (1976) The β-lactamases of Gram-negative bacteria and their rôle in resistance to β-lactam antibiotics. J Antimicrob Chemother 2: 115-157
43. Tan C, Phillip SR, Srimani JK, Riccione KA, Prasada S, Kuehn M, You L, (2012) The inoculum effect and band-pass bacterial response to periodic antibiotic treatment. Mol Syst Biol 8: 617
44. Tan L, Serene S, Chao HX, Gore J, (2011) Hidden randomness between fitness landscapes limits reverse evolution. Phys Rev Lett 106: 198102
45. Tanouchi Y, Pai A, Buchler NE, You L, (2012) Programming stress-induced altruistic death in engineered bacteria. Mol Syst Biol 8: 626
46. Walsh C, (2000) Molecular mechanisms that confer antibacterial drug resistance. Nature 406: 775-781
47. Wang X, Minasov G, Shoichet BK, (2002) Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J Mol Biol 320: 85-95
48. Weinreich DM, Delaney NF, DePristo MA, Hartl DL, (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-114
49. Wiegand I, Hilpert K, Hancock REW, (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3: 163-175
50. Wiuff C, Zappala RM, Regoes RR, Garner KN, Baquero F, Levin BR, (2005) Phenotypic tolerance: antibiotic enrichment of noninherited resistance in bacterial populations. Antimicrob Agents Chemother 49: 1483-1494
51. Yao Z, Kahne D, Kishony R, (2012) Distinct single-cell morphological dynamics under beta-lactam antibiotics. Mol Cell 48: 705-712
52. Yeh PJ, Hegreness MJ, Aiden AP, Kishony R, (2009) Drug interactions and the evolution of antibiotic resistance. Nat Rev Microbiol 7: 460-466
53. Yurtsev EA, Chao HX, Datta MS, Artemova T, Gore J, (2013) Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids. Mol Syst Biol 9: 683
54. Zimmermann W, Rosselet A, (1977) Function of the outer membrane of Escherichia coli as a permeability barrier to beta-lactam antibiotics. Antimicrob Agents Chemother 12: 368-372