Laboratory divergence of Methylobacterium extorquens AM1 through unintended domestication and past selection for antibiotic resistance

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Carroll, Sean Michael ^a   Xue, Katherine S ^b   Marx, Christopher J ^a,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD COLLEGE   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Antibiotic resistance; Laboratory domestication; Methylobacterium extorquens AM1; Rifamycin; Strain integrity; Whole genome sequencing

Indexed keywords

ANTIBIOTIC AGENT; DNA; RIFAMYCIN; RNA POLYMERASE BETA SUBUNIT;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATE; CONTROLLED STUDY; DOMESTICATION; FREEZE DRYING; GENE SEQUENCE; GENETIC SELECTION; GENOMICS; INDEL MUTATION; LABORATORY; METHYLOBACTERIUM EXTORQUENS; NONHUMAN; NUTRIENT; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIVERSITY;

METHYLOBACTERIUM EXTORQUENS;

DRUG RESISTANCE, BACTERIAL; GENETIC VARIATION; GENOTYPE; METHYLOBACTERIUM EXTORQUENS; PHENOTYPE; SELECTION, GENETIC; SERIAL PASSAGE;

EID: 84894472994     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-2     Document Type: Article

References (62)

1. Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-gamma-dl-glutamic acid production and biofilm formation. Stanley NR, Lazazzera BA, Mol Microbiol 2005 57 1143 1158 10.1111/j.1365-2958.2005.04746.x 16091050 (Pubitemid 41139872)
2. Swarming motility in undomesticated Bacillus subtilis. Kearns DB, Losick R, Mol Microbiol 2003 49 581 590 12864845 (Pubitemid 36918682)
3. Fruiting body formation by Bacillus subtilis. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R, Proc Natl Acad Sci U S A 2001 98 11621 11626 10.1073/pnas.191384198 11572999 (Pubitemid 32928778)
4. Genetic diversity among offspring from archived Salmonella enterica ssp. enterica Serovar Typhimurium (Demerec Collection): In search of survival strategies. Eisenstark A, Annu Rev Microbiol 2010 64 277 292 10.1146/annurev.micro.091208.073614 20825350
5. Genomic diversification among archival strains of Salmonella enterica serovar typhimurium LT7. Liu G-R, Edwards K, Eisenstark A, Fu Y-M, Liu W-Q, Sanderson KE, Johnston RN, Liu S-L, J Bacteriol 2003 185 2131 2142 10.1128/JB.185.7.2131-2142.2003 12644482 (Pubitemid 36363173)
6. Genomic changes arising in long-term stab cultures of Escherichia coli. Faure D, Frederick R, Wloch D, Portier P, Blot M, Adams J, J Bacteriol 2004 186 6437 6442 10.1128/JB.186.19.6437-6442.2004 15375124 (Pubitemid 39258125)
7. Insertion sequence-related genetic variation in resting Escherichia coli K-12. Naas T, Blot M, Fitch WM, Arber W, Genetics 1994 136 721 730 7911771 (Pubitemid 24085625)
8. Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12. Naas T, Blot M, Fitch WM, Arber W, Mol Biol Evol 1995 12 198 207 7700149
9. Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage. Davidson CJ, White AP, Surette MG, ISME J 2008 2 293 307 10.1038/ismej.2008.4 18256702 (Pubitemid 351334278)
10. The uncertain consequences of transferring bacterial strains between laboratories-rpoS instability as an example. Spira B, de Almeida Toledo R, Maharjan RP, Ferenci T, BMC Microbiol 2011 11 248 10.1186/1471-2180-11-248 22067413
11. The nature of laboratory domestication changes in freshly isolated Escherichia coli strains. Eydallin G, Ryall B, Maharjan R, Ferenci T, Environ Microbiol 2013 doi:10.1111/1462-2920.12208
12. Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution. Bachmann H, Starrenburg MJC, Molenaar D, Kleerebezem M, van Hylckama Vlieg JET, Genome Res 2012 22 115 124 10.1101/gr.121285.111 22080491
13. Domestication of wild Saccharomyces cerevisiae is accompanied by changes in gene expression and colony morphology. Kuthan M, Devaux F, Janderová B, Slaninová I, Jacq C, Palková Z, Mol Microbiol 2003 47 745 754 10.1046/j.1365-2958.2003.03332.x 12535073 (Pubitemid 36114982)
14. Whole genome sequencing highlights genetic changes associated with laboratory domestication of C. elegans. Weber KP, De S, Kozarewa I, Turner DJ, Babu MM, de Bono M, PLoS One 2010 5 13922 10.1371/journal.pone.0013922 21085631
15. Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI, Nature 2011 477 321 325 10.1038/nature10378 21849976
16. Recurrent DNA copy number variation in the laboratory mouse. Egan CM, Sridhar S, Wigler M, Hall IM, Nat Genet 2007 39 1384 1389 10.1038/ng.2007.19 17965714 (Pubitemid 350034999)
17. Genome-wide single-nucleotide polymorphism analysis defines haplotype patterns in mouse. Wiltshire T, Proc Natl Acad Sci U S A 2003 100 3380 3385 10.1073/pnas.0130101100 12612341 (Pubitemid 36356592)
18. Microbial growth on C§ssub§1§esub§ compounds. 1. Isolation and characterization of Pseudomonas AM1. Peel D, Quayle JR, Biochem J 1961 81 465 14484877
19. The metabolism of lactate and pyruvate by Pseudomonas AM1. Salem AR, Wagner C, Hacking AJ, Quayle JR, J Gen Microbiol 1973 76 375 388 10.1099/00221287-76-2-375 4723074
20. Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. Chistoserdova L, Chen S-W, Lapidus A, Lidstrom ME, J Bacteriol 2003 185 2980 2987 10.1128/JB.185.10.2980-2987.2003 12730156 (Pubitemid 36539093)
21. Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of C§ssub§1§esub§ compounds from natural and industrial sources. Vuilleumier S, Chistoserdova L, Lee M-C, Bringel F, Lajus A, Zhou Y, Gourion B, Barbe V, Chang J, Cruveiller S, Dossat C, Gillett W, Gruffaz C, Haugen E, Hourcade E, Levy R, Mangenot S, Muller E, Nadalig T, Pagni M, Penny C, Peyraud R, Robinson DG, Roche D, Rouy Z, Saenampechek C, Salvignol G, Vallenet D, Wu Z, Marx CJ, et al. PLoS One 2009 4 5584 10.1371/journal.pone.0005584 19440302
22. Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Marx CJ, Lidstrom ME, Biotechniques 2002 33 1062 1067 12449384 (Pubitemid 35285540)
23. Development of a broad-host-range sacB-based vector for unmarked allelic exchange. Marx CJ, BMC Research Notes 2008 1 1 10.1186/1756-0500-1-1 18710539
24. Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria. Marx CJ, Lidstrom ME, Microbiology 2001 147 2065 2075 11495985 (Pubitemid 32785488)
25. Development of an insertional expression vector system for Methylobacterium extorquens AM1 and generation of null mutants lacking mtdA and/or fch. Marx CJ, Lidstrom ME, Microbiology 2004 150 9 19 10.1099/mic.0.26587-0 14702393 (Pubitemid 38111466)
26. A novel pair of inducible expression vectors for use in Methylobacterium extorquens. Chubiz LM, Purswani J, Carroll SM, Marx CJ, BMC Res Notes 2013 6 183 10.1186/1756-0500-6-183 23648175
27. Development of an optimized medium, strain and high-throughput culturing methods for Methylobacterium extorquens. Delaney NF, Kaczmarek ME, Ward LM, Swanson PK, Lee M-C, Marx CJ, PLoS One 2013 8 62957 10.1371/journal.pone.0062957 23646164
28. Genome-scale reconstruction and system level investigation of the metabolic network of Methylobacterium extorquens AM1. Peyraud R, Schneider K, Kiefer P, Massou S, Vorholt JA, Portais J-C, BMC Syst Biol 2011 5 189 10.1186/1752-0509-5-189 22074569
29. A systems biology approach uncovers cellular strategies used by Methylobacterium extorquens AM1 during the switch from multi- to single-carbon growth. Skovran E, Crowther GJ, Guo X, Yang S, Lidstrom ME, PLoS One 2010 5 14091 10.1371/journal.pone.0014091 21124828
30. Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Lee M-C, Chou H-H, Marx CJ, Evolution 2009 63 2816 2830 10.1111/j.1558-5646.2009.00757.x 19545267
31. Diminishing returns epistasis among beneficial mutations decelerates adaptation. Chou H-H, Chiu H-C, Delaney NF, Segrè D, Marx CJ, Science 2011 332 1190 1192 10.1126/science.1203799 21636771
32. Repeated, selection-driven genome reduction of accessory genes in experimental populations. Lee M-C, Marx CJ, PLoS Genet 2012 8 1002651 10.1371/journal.pgen.1002651 22589730
33. Evolution after introduction of a novel metabolic pathway consistently leads to restoration of wild-type physiology. Carroll SM, Marx CJ, PLoS Genet 2013 9 1003427 10.1371/journal.pgen.1003427 23593025
34. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, Mering Von C, Vorholt JA, Proc Natl Acad Sci U S A 2009 106 16428 16433 10.1073/pnas.0905240106 19805315
35. Competitiveness of diverse Methylobacterium strains in the phyllosphere of Arabidopsis thaliana and identification of representative models, including M. extorquens PA1. Knief C, Frances L, Vorholt JA, Microb Ecol 2010 60 440 452 10.1007/s00248-010-9725-3 20700590
36. Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Jourand P, Giraud E, Béna G, Sy A, Willems A, Gillis M, Dreyfus B, de Lajudie P, Int J Syst Evol Microbiol 2004 54 2269 2273 10.1099/ijs.0.02902-0 15545469 (Pubitemid 39585416)
37. Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides x nigra DN34). Van Aken B, Peres CM, Doty SL, Yoon JM, Schnoor JL, Int J Syst Evol Microbiol 2004 54 1191 1196 10.1099/ijs.0.02796-0 15280290 (Pubitemid 39139838)
38. Isolation and initial characterization of aerobic chloromethane-utilizing bacteria. Doronina NV, Sokolov AP, Trotsenko YA, FEMS Microbiol Lett 1996 142 179 183 10.1111/j.1574-6968.1996.tb08427.x (Pubitemid 26279142)
39. Specialized bacterial strains for the removal of dichloromethane from industrial waste. Gälli R, Leisinger T, Conservation & Recycling 1985 8 91 100 10.1016/0361-3658(85)90028-1 (Pubitemid 15037315)
40. Biotechnological potential of the ethylmalonyl-CoA pathway. Alber BE, Appl Microbiol Biotechnol 2011 89 17 25 10.1007/s00253-010-2873-z 20882276
41. Methanol-based industrial biotechnology: current status and future perspectives of methylotrophic bacteria. Schrader J, Schilling M, Holtmann D, Sell D, Filho MV, Marx A, Vorholt JA, Trends Biotechnol 2009 27 107 115 10.1016/j.tibtech.2008.10.009 19111927
42. Methanol and carbon dioxide incorporation by Pseudomonas sp. AM1. Quayle J, Peel D, Biochem J 1960 76 3P
43. Complete genome sequences of six strains of the genus Methylobacterium. Marx CJ, Bringel F, Chistoserdova L, Moulin L, Farhan Ul Haque M, Fleischman DE, Gruffaz C, Jourand P, Knief C, Lee M-C, Muller EEL, Nadalig T, Peyraud R, Roselli S, Russ L, Goodwin LA, Ivanova N, Kyrpides N, Lajus A, Land ML, Médigue C, Mikhailova N, Nolan M, Woyke T, Stolyar S, Vorholt JA, Vuilleumier S, J Bacteriol 2012 194 4746 4748 10.1128/JB.01009-12 22887658
44. Clarity: an open-source manager for laboratory automation. Delaney NF, Rojas Echenique JI, Marx CJ, J Lab Autom 2013 18 171 177 10.1177/ 2211068212460237 23032169
45. Molecular cloning of a malyl coenzyme A lyase gene from Pseudomonas sp. strain AM1, a facultative methylotroph. Fulton GL, Nunn DN, Lidstrom ME, J Bacteriol 1984 160 718 723 6094488 (Pubitemid 15214290)
46. The biological cost of mutational antibiotic resistance: any practical conclusions? Andersson DI, Curr Opin Microbiol 2006 9 461 465 10.1016/j.mib.2006.07.002 16890008 (Pubitemid 44397630)
47. Rifamycin: mode of action, resistance, and biosynthesis. Floss HG, Yu T-W, Chem Rev 2005 105 621 632 10.1021/cr030112j 15700959 (Pubitemid 40351636)
48. The increased sensitivity of rifamycin-resistant mutants of Methylobacterium AM1 to a variety of antimicrobial agents. Goodwin PM, Piercy R, Stone S, Lett Appl Microbiol 1988 7 99 101 10.1111/j.1472-765X.1988.tb01262.x (Pubitemid 19007897)
49. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Schrag SJ, Perrot V, Levin BR, Proc Biol Sci 1997 264 1287 1291 10.1098/rspb.1997.0178 9332013 (Pubitemid 27445226)
50. Methanol metabolism in pseudomonad C. Stieglitz B, Mateles RI, J Bacteriol 1973 114 390 398 4349032
51. Long-term survival during stationary phase: evolution and the GASP phenotype. Finkel SE, Nat Rev Micro 2006 4 113 120 10.1038/nrmicro1340 (Pubitemid 43158154)
52. Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. Chou H-H, Berthet J, Marx CJ, PLoS Genet 2009 5 1000652 10.1371/journal.pgen.1000652 19763169
53. Multiple long-term, experimentally-evolved populations of Escherichia coli acquire dependence upon citrate as an iron chelator for optimal growth on glucose. Leiby N, Harcombe WR, Marx CJ, BMC Evol Biol 2012 12 1 1 10.1186/1471-2148-12-1 22214193
54. Laboratory-dependent bacterial ecology: a cautionary tale. O'Keefe KJ, Morales NM, Ernstberger H, Benoit G, Turner PE, Appl Environ Microbiol 2006 72 3032 3035 10.1128/AEM.72.4.3032-3035.2006 16598013
55. Good codons, bad transcript: large reductions in gene expression and fitness arising from synonymous mutations in a key enzyme. Agashe D, Martinez-Gomez NC, Drummond DA, Marx CJ, Mol Biol Evol 2013 30 549 560 10.1093/molbev/mss273 23223712
56. Optimization of gene expression through divergent mutational paths. Chou H-H, Marx CJ, Cell Reports 2012 1 133 140 10.1016/j.celrep.2011.12.003 22832162
57. Preparation of genomic DNA from bacteria. Wilson K, Curr Protoc Mol Biol 2001 00:2.4.1-2.4.5
58. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF, Nature 2009 461 1243 1247 10.1038/nature08480 19838166
59. Fast gapped-read alignment with Bowtie 2. Langmead B, Salzberg SL, Nat Meth 2012 9 357 359 10.1038/nmeth.1923
60. ABySS: a parallel assembler for short read sequence data. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I, Genome Res 2009 19 1117 1123 10.1101/gr.089532.108 19251739
61. Geneious version 6.1.6, created by Biomatters http://www.geneious.com
62. MicroScope - an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S, Lajus A, Le Fèvre F, Longin C, Mornico D, Roche D, Rouy Z, Salvignol G, Scarpelli C, Thil Smith AA, Weiman M, Médigue C, Nucleic Acids Res 2013 41 Database issue 636 D647 23193269