Effective use of a horizontally-transferred pathway for dichloromethane catabolism requires post–transfer refinement

eLife

Volumn 3, Issue November, 2014, Pages 1-16

  Michener, Joshua K ^a   Neves, Aline A Camargo ^a,b   Vuilleumier, Stéphane ^c   Bringel, Françoise ^c   Marx, Christopher J ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICHLOROMETHANE;

ALLELE; ARTICLE; BACTERIUM ISOLATION; EVOLUTIONARY HOMOLOGY; FLOW CYTOMETRY; GENE MUTATION; GROWTH RATE; HORIZONTAL GENE TRANSFER; METHYLOBACTERIUM; MICROBIAL DEGRADATION; NONHUMAN; PH MEASUREMENT; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; BACTERIAL GENE; GENETICS; METABOLISM; MUTATION;

BACTERIA (MICROORGANISMS); METHYLOBACTERIUM;

ALLELES; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; METHYLENE CHLORIDE; METHYLOBACTERIUM; MUTATION;

EID: 84936138027     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.04279     Document Type: Article

References (62)

1. Accardi A, Miller C. 2004. Secondary active transport mediated by a prokaryotic homologue of Cl C Cl-channels. Nature 427:803-807. doi: 10.1038/nature02314.
2. Atwood KC, Schneider LK, Ryan FJ. 1951. Periodic selection in Escherichia coli. Proceedings of the National Academy of Sciences of USA 37:146-155. doi: 10.1073/pnas.37.3.146.
3. Bernhardt R, Urlacher VB. 2014. Cytochromes P450 as promising catalysts for biotechnological application: chances and limitations. Applied Microbiology and Biotechnology 98:6185-6203. doi: 10.1007/s00253-014-5767-7.
4. Blount ZD, Barrick JE, Davidson CJ, Lenski RE. 2012. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489:513-518. doi: 10.1038/nature11514.
5. Chang MC, Eachus RA, Trieu W, Ro DK, Keasling JD. 2007. Engineering Escherichia coli for production of functionalized terpenoids using plant P450s. Nature Chemical Biology 3:274-277. doi: 10.1038/nchembio875.
6. Chistoserdova L. 2011. Modularity of methylotrophy, revisited. Environmental Microbiology 13:2603-2622. doi: 10.1111/j.1462-2920.2011.02464.x.
7. Chou HH, Chiu HC, Delaney NF, Segre D, Marx CJ. 2011. Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332:1190-1192. doi: 10.1126/science.1203799.
8. Chou HH, Delaney NF, Draghi JA, Marx CJ. 2014. Mapping the fitness landscape of gene expression uncovers the cause of antagonism and sign epistasis between adaptive mutations. PLOS Genetics 10:e1004149. doi: 10.1371/ journal.pgen.1004149.
9. Dalal K, Duong F. 2009. The Sec Y complex forms a channel capable of ionic discrimination. EMBO Reports 10:762-768. doi: 10.1038/embor.2009.87.
10. Deatherage DE, Barrick JE. 2014. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods in Molecular Biology 1151:165-188. doi: 10.1007/978-1-4939-0554-6_12.
11. Delaney NF, Kaczmarek ME, Ward LM, Swanson PK, Lee MC, Marx CJ. 2013a. Development of an optimized medium, strain and high-throughput culturing methods for Methylobacterium extorquens. PLOS ONE 8:e62957. doi: 10.1371/journal.pone.0062957.
12. Delaney NF, Rojas Echenique JI, Marx CJ. 2013b. Clarity: an open-source manager for laboratory automation. Journal of Laboratory Automation 18:171-177. doi: 10.1177/2211068212460237.
13. Elena SF, Lenski RE. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews. Genetics 4:457-469. doi: 10.1038/nrg1088.
14. Emr SD, Hanley-Way S, Silhavy TJ. 1981. Suppressor mutations that restore export of a protein with a defective signal sequence. Cell 23:79-88. doi: 10.1016/0092-8674(81)90272-5.
15. Firsova JE, Doronina NV, Trotsenko YA. 2010. Analysis of the key functional genes in new aerobic degraders of dichloromethane. Nature Reviews. Microbiology 79:66-72. doi: 10.1134/S0026261710010091.
16. Fong SS, Burgard AP, Herring CD, Knight EM, Blattner FR, Maranas CD, Palsson BO. 2005. In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnology and Bioengineering 91:643-648. doi: 10.1002/bit.20542.
17. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107-1111. doi: 10.1126/science.1220761.
18. Fulton GL, Nunn DN, Lidstrom ME. 1984. Molecular cloning of a malyl coenzyme A lyase gene from Pseudomonas sp. strain AM1, a facultative methylotroph. Journal of Bacteriology 160:718-723.
19. Gälli R, Leisinger T. 1985. Specialized bacterial strains for the removal of dichloromethane from industrial waste. Conservation & Recycling 8:91-100.
20. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA III, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nature Methods 6:343-345. doi: 10.1038/nmeth.1318.
21. Gogarten JP, Doolittle WF, Lawrence JG. 2002. Prokaryotic evolution in light of gene transfer. Molecular Biology and Evolution 19:2226-2238. doi: 10.1093/oxfordjournals.molbev.a004046.
22. Ikuma K, Gunsch CK. 2013. Successful genetic bioaugmentation with Pseudomonas putida for toluene degradation in soil columns. Environmental Chemistry Letters 11:365-370. doi: 10.1007/s10311-013-0416-4.
23. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, Fukui K. 2007. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. Journal of Bacteriology 189:950-957. doi: 10.1128/JB.01294-06.
24. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. 2012. Experimental evolution. Trends in Ecology & Evolution 27:547-560. doi: 10.1016/j.tree.2012.06.001.
25. Kayser MF, Stumpp MT, Vuilleumier S. 2000. DNA polymerase I is essential for growth of Methylobacterium dichloromethanicum DM4 with dichloromethane. Journal of Bacteriology 182:5433-5439. doi: 10.1128/ JB.182.19.5433-5439.2000.
26. Kayser MF, Vuilleumier S. 2001. Dehalogenation of dichloromethane by dichloromethane dehalogenase/ glutathione S-transferase leads to formation of DNA adducts. Journal of Bacteriology 183:5209-5212. doi: 10.1128/JB.183.17.5209-5212.2001.
27. Kayser MF, Ucurum Z, Vuilleumier S. 2002. Dichloromethane metabolism and C1 utilization genes in Methylobacterium strains. Nature Reviews. Microbiology 148:1915-1922.
28. Kim J, Copley SD. 2012. Inhibitory cross-talk upon introduction of a new metabolic pathway into an existing metabolic network. Proceedings of the National Academy of Sciences of USA 109:E2856-E2864. doi: 10.1073/ pnas.1208509109.
29. Kizer L, Pitera DJ, Pfleger BF, Keasling JD. 2008. Application of functional genomics to pathway optimization for increased isoprenoid production. Applied and Environmental Microbiology 74:3229-3241. doi: 10.1128/ AEM.02750-07.
30. Kvitek DJ, Sherlock G. 2011. Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLOS Genetics 7:e1002056. doi: 10.1371/journal.pgen. 1002056.
31. Lee MC, Marx CJ. 2012. Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLOS Genetics 8:e1002651. doi: 10.1371/journal.pgen.1002651.
32. Lee DH, Palsson BØ. 2010. Adaptive evolution of Escherichia coli K-12 MG1655 during growth on a Nonnative carbon source, L-1,2-propanediol. Applied and Environmental Microbiology 76:4158-4168. doi: 10.1128/ AEM.00373-10.
33. Lee MC, Chou HH, Marx CJ. 2009. Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63:2816-2830. doi: 10.1111/j.1558-5646.2009.00757.x.
34. Lee SM, Jellison T, Alper HS. 2012. Directed evolution of xylose isomerase for improved xylose catabolism and fermentation in the yeast Saccharomyces cerevisiae. Applied and Environmental Microbiology 78:5708-5716. doi: 10.1128/AEM.01419-12.
35. Marx CJ, Bringel F, Chistoserdova L, Moulin L, Farhan Ul Haque M, Fleischman DE, Gruffaz C, Jourand P, Knief C, Lee MC, Muller EE, 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. 2012. Complete genome sequences of six strains of the genus Methylobacterium. Journal of Bacteriology 194:4746-4748. doi: 10.1128/ JB.01009-12.
36. Marx CJ. 2008. Development of a broad-host-range sac B-based vector for unmarked allelic exchange. BMC Research Notes 1:1. doi: 10.1186/1756-0500-1-1.
37. Michener JK, Nielsen J, Smolke CD. 2012. Identification and treatment of heme depletion attributed to overexpression of a lineage of evolved P450 monooxygenases. Proceedings of the National Academy of Sciences of USA 109:19504-19509. doi: 10.1073/pnas.1212287109.
38. Michener JK, Vuilleumier S, Bringel F, Marx CJ. 2014. Phylogeny poorly predicts the utility of a challenging horizontally transferred gene in Methylobacterium strains. Journal of Bacteriology 196:2101-2107. doi: 10.1128/ JB.00034-14.
39. Muller EE, Bringel F, Vuilleumier S. 2011a. Dichloromethane-degrading bacteria in the genomic age. Research in Microbiology 162:869-876. doi: 10.1016/j.resmic.2011.01.008.
40. Muller EE, Hourcade E, Louhichi-Jelail Y, Hammann P, Vuilleumier S, Bringel F. 2011b. Functional genomics of dichloromethane utilization in Methylobacterium extorquens DM4. Environmental Microbiology 13:2518-2535. doi: 10.1111/j.1462-2920.2011.02524.x.
41. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304. doi: 10.1038/35012500.
42. Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V. 2013. Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria. PLOS Genetics 9:e1003764. doi: 10.1371/ journal.pgen.1003764.
43. Quandt EM, Deatherage DE, Ellington AD, Georgiou G, Barrick JE. 2014. Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in Escherichia coli. Proceedings of the National Academy of Sciences of USA 111:2217-2222. doi: 10.1073/pnas.1314561111.
44. Rahn-Lee L, Gorbatyuk B, Skovgaard O, Losick R. 2009. The conserved sporulation protein Yne E inhibits DNA replication in Bacillus subtilis. Journal of Bacteriology 191:3736-3739. doi: 10.1128/JB.00216-09.
45. Ro DK, Ouellet M, Paradise EM, Burd H, Eng D, Paddon CJ, Newman JD, Keasling JD. 2008. Induction of multiple pleiotropic drug resistance genes in yeast engineered to produce an increased level of anti-malarial drug precursor, artemisinic acid. BMC Biotechnology 8:83. doi: 10.1186/1472-6750-8-83.
46. Rokyta DR, Joyce P, Caudle SB, Miller C, Beisel CJ, Wichman HA. 2011. Epistasis between beneficial mutations and the phenotype-to-fitness map for a ss DNA virus. PLOS Genetics 7:e1002075. doi: 10.1371/journal. pgen.1002075.
47. Schmid-Appert M, Zoller K, Traber H, Vuilleumier S, Leisinger T. 1997. Association of newly discovered IS elements with the dichloromethane utilization genes of methylotrophic bacteria. Nature Reviews. Microbiology 143:2557-2567. doi: 10.1099/00221287-143-8-2557.
48. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, Polz MF, Alm EJ. 2012. Population genomics of early events in the ecological differentiation of bacteria. Science 336:48-51. doi: 10.1126/ science.1218198.
49. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480:241-244. doi: 10.1038/nature10571.
50. Smith MA, Clemons WM Jr, De Mars CJ, Flower AM. 2005. Modeling the effects of prl mutations on the Escherichia coli Sec Y complex. Journal of Bacteriology 187:6454-6465. doi: 10.1128/JB.187.18.6454-6465.2005.
51. Springael D, Top EM. 2004. Horizontal gene transfer and microbial adaptation to xenobiotics: new types of mobile genetic elements and lessons from ecological studies. Trends in Microbiology 12:53-58. doi: 10.1016/ j.tim.2003.12.010.
52. Sun H, Tsunenari T, Yau KW, Nathans J. 2002. The vitelliform macular dystrophy protein defines a new family of chloride channels. Proceedings of the National Academy of Sciences of USA 99:4008-4013. doi: 10.1073/ pnas.052692999.
53. Top EM, Springael D, Boon N. 2002. Catabolic mobile genetic elements and their potential use in bioaugmentation of polluted soils and waters. FEMS Microbiology Ecology 42:199-208. doi: 10.1111/j.1574-6941.2002. tb01009.x.
54. Traverse CC, Mayo-Smith LM, Poltak SR, Cooper VS. 2013. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proceedings of the National Academy of Sciences of USA 110:E250-E259. doi: 10.1073/pnas.1207025110.
55. Trinh CT, Srienc F. 2009. Metabolic engineering of Escherichia coli for efficient conversion of glycerol to ethanol. Applied and Environmental Microbiology 75:6696-6705. doi: 10.1128/AEM.00670-09.
56. Tsunenari T, Sun H, Williams J, Cahill H, Smallwood P, Yau KW, Nathans J. 2003. Structure-function analysis of the bestrophin family of anion channels. The Journal of Biological Chemistry 278:41114-41125. doi: 10.1074/jbc. M306150200.
57. Van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA. 2004. X-ray structure of a protein-conducting channel. Nature 427:36-44.
58. Verwaal R, Jiang Y, Wang J, Daran JM, Sandmann G, van den Berg JA, van Ooyen AJ. 2010. Heterologous carotenoid production in Saccharomyces cerevisiae induces the pleiotropic drug resistance stress response. Yeast 27:983-998. doi: 10.1002/yea.1807.
59. Vuilleumier S, Chistoserdova L, Lee MC, 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, Vorholt JA, Olson MV, Kaul R, Weissenbach J, Médigue C, Lidstrom ME. 2009. Methylobacterium genome sequences: a reference blueprint to Investigate microbial metabolism of C1 compounds from natural and industrial sources. PLOS ONE 4:e5584. doi: 10.1371/journal.pone.0005584.
60. Winkler J, Kao KC. 2012. Harnessing recombination to speed adaptive evolution in Escherichia coli. Metabolic Engineering 14:487-495. doi: 10.1016/j.ymben.2012.07.004.
61. Wong A, Rodrigue N, Kassen R. 2012. Genomics of adaptation during experimental evolution of the opportunistic pathogen Pseudomonas aeruginosa. PLOS Genetics 8:e1002928. doi: 10.1371/journal.pgen.1002928.
62. Yadid I, Rudolph J, Hlouchova K, Copley SD. 2013. Sequestration of a highly reactive intermediate in an evolving pathway for degradation of pentachlorophenol. Proceedings of the National Academy of Sciences of USA 110:E2182-E2190. doi: 10.1073/pnas.1214052110.