Phylogeny poorly predicts the utility of a challenging horizontally transferred gene in Methylobacterium strains

Journal of Bacteriology

Volumn 196, Issue 11, 2014, Pages 2101-2107

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

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; DICHLOROMETHANE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; ENERGY RESOURCE; GENE DISRUPTION; HORIZONTAL GENE TRANSFER; METHYLOBACTERIUM; METHYLOBACTERIUM EXTORQUENS; MOLECULAR PHYLOGENY; NONHUMAN; PRIORITY JOURNAL; RECIPIENT; STRESS;

GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE TRANSFER, HORIZONTAL; HYDROGEN-ION CONCENTRATION; LYASES; METHYLENE CHLORIDE; METHYLOBACTERIUM; PHYLOGENY;

EID: 84899768571     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00034-14     Document Type: Article

References (46)

1. Gogarten JP, Doolittle WF, Lawrence JG. 2002. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19:2226-2238. http://dx.doi.org/10.1093/oxfordjournals.molbev.a004046.
2. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304. http://dx.doi.org/10.1038/35012500.
3. Wiedenbeck J, Cohan FM. 2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol. Rev. 35:957-976. http://dx.doi.org/10.1111/j.1574-6976.2011.00292.x.
4. Popa O, Dagan T. 2011. Trends and barriers to lateral gene transfer in prokaryotes. Curr. Opin. Microbiol. 14:615-623. http://dx.doi.org/10.1016/j.mib.2011.07.027.
5. Thomas CM, Nielsen KM. 2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3:711-721. http://dx.doi.org/10.1038/nrmicro1234.
6. 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. http://dx.doi.org/10.1126/science.1218198.
7. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in Staphylococci by targeting DNA. Science 322: 1843-1845. http://dx.doi.org/10.1126/science.1165771.
8. Fraser C, Hanage WP, Spratt BG. 2007. Recombination and the nature of bacterial speciation. Science 315:476-480. http://dx.doi.org/10.1126/science.1127573.
9. Popa O, Hazkani-Covo E, Landan G, Martin W, Dagan T. 2011. Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. Genome Res. 21:599-609. http://dx.doi.org/10.1101/gr.115592.110.
10. Tuller T, Girshovich Y, Sella Y, Kreimer A, Freilich S, Kupiec M, Gophna U, Ruppin E. 2011. Association between translation efficiency and horizontal gene transfer within microbial communities. Nucleic Acids Res. 39:4743-4755. http://dx.doi.org/10.1093/nar/gkr054.
11. 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. http://dx.doi.org/10.1038/nature10571.
12. Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, Rubin EM. 2007. Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318:1449-1452. http://dx.doi.org/10.1126/science.1147112.
13. Chou HH, Chiu HC, Delaney NF, Segre D, Marx CJ. 2011. Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332:1190-1192. http://dx.doi.org/10.1126/science.1203799.
14. Kim J, Copley SD. 2012. Inhibitory cross-talk upon introduction of a new metabolic pathway into an existing metabolic network. Proc. Natl. Acad. Sci. U. S. A. 109:E2856-E2864. http://dx.doi.org/10.1073/pnas.1208509109.
15. Gälli R, Leisinger T. 1985. Specialized bacterial strains for the removal of dichloromethane from industrial waste. Conserv. Recycling 8:91-100. http://dx.doi.org/10.1016/0361-3658(85)90028-1.
16. Muller EE, Bringel F, Vuilleumier S. 2011. Dichloromethane-degrading bacteria in the genomic age. Res. Microbiol. 162:869-876. http://dx.doi.org/10.1016/j.resmic.2011.01.008.
17. La Roche SD, Leisinger T. 1990. Sequence analysis and expression of the bacterial dichloromethane dehalogenase structural gene, a member of the glutathione S-transferase supergene family. J. Bacteriol. 172:164-171.
18. 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. Microbiol. 143:2557-2567. http://dx.doi.org/10.1099/00221287-143-8-2557.
19. 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, 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. http://dx.doi.org/10.1371/journal.pone.0005584.
20. Gälli R, Leisinger T. 1988. Plasmid analysis and cloning of the dichloromethane-utilization genes of Methylobacterium sp. DM4. J. Gen. Microbiol. 134:943-952.
21. Kayser MF, Ucurum Z, Vuilleumier S. 2002. Dichloromethane metabolism and C1 utilization genes in Methylobacterium strains. Microbiology 148:1915-1922. http://mic.sgmjournals.org/content/148/6/1915.long.
22. Torgonskaya ML, Doronina NV, Hourcade E, Trotsenko YA, Vuilleumier S. 2011. Chloride-associated adaptive response in aerobic methylotrophic dichloromethane-utilising bacteria. J. Basic Microbiol. 51:296-303. http://dx.doi.org/10.1002/jobm.201000280.
23. Muller EE, Hourcade E, Louhichi-Jelail Y, Hammann P, Vuilleumier S, Bringel F. 2011. Functional genomics of dichloromethane utilization in Methylobacterium extorquens DM4. Environ. Microbiol. 13:2518-2535. http://dx.doi.org/10.1111/j.1462-2920.2011.02524.x.
24. Evans GJ, Ferguson GP, Booth IR, Vuilleumier S. 2000. Growth inhibition of Escherichia coli by dichloromethane in cells expressing dichloromethane dehalogenase/glutathione S-transferase. Microbiology 146: 2967-2975. http://mic.sgmjournals.org/content/146/11/2967.long.
25. Kayser MF, Vuilleumier S. 2001. Dehalogenation of dichloromethane by dichloromethane dehalogenase/glutathione S-transferase leads to formation of DNA adducts. J. Bacteriol. 183:5209-5212. http://dx.doi.org/10.1128/JB.183.17.5209-5212.2001.
26. Kayser MF, Stumpp MT, Vuilleumier S. 2000. DNA polymerase I is essential for growth of Methylobacterium dichloromethanicum DM4 with dichloromethane. J. Bacteriol. 182:5433-5439. http://dx.doi.org/10.1128/JB.182.19.5433-5439.2000.
27. Gisi D, Leisinger T, Vuilleumier S. 1999. Enzyme-mediated dichloromethane toxicity and mutagenicity of bacterial and mammalian dichloromethane-active glutathione S-transferases. Arch. Toxicol. 73:71-79. http://dx.doi.org/10.1007/s002040050589.
28. Vorholt JA, Marx CJ, Lidstrom ME, Thauer RK. 2000. Novel formaldehyde-activating enzyme in Methylobacterium extorquens AM1 required for growth on methanol. J. Bacteriol. 182:6645-6650. http://dx.doi.org/10.1128/JB.182.23.6645-6650.2000.
29. Delaney NF, Kaczmarek ME, Ward LM, Swanson PK, Lee MC, Marx CJ. 2013. Development of an optimized medium, strain and highthroughput culturing methods for Methylobacterium extorquens. PLoS One 8:e62957. http://dx.doi.org/10.1371/journal.pone.0062957.
30. Marx CJ, Lidstrom ME. 2002. Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Biotechniques 33: 1062-1067. http://www.biotechniques.com/multimedia/archive/00010/0 2335rr01_10092a.pdf.
31. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA. 2000. The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79:2199-2208. http://dx.doi.org/10.1016/S0006-3495(00)76468-X.
32. Lee MC, Chou HH, Marx CJ. 2009. Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63:2816-2830. http://dx.doi.org/10.1111/j.1558-5646.2009.00757.x.
33. Marx CJ. 2008. Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res. Notes 1:1. http://dx.doi.org/10.1186/1756-0500-1-1.
34. Fulton GL, Nunn DN, Lidstrom ME. 1984. Molecular cloning of a malyl coenzyme A lyase gene from Pseudomonas sp. strain AM1, a facultative methylotroph. J. Bacteriol. 160:718-723.
35. Jörg G, Bertau M. 2004. Thiol-tolerant assay for quantitative colorimetric determination of chloride released from whole-cell biodehalogenations. Anal. Biochem. 328:22-28. http://dx.doi.org/10.1016/j.ab.2004.01.027.
36. Vuilleumier S, Leisinger T. 1996. Protein engineering studies of dichloromethane dehalogenase/glutathione S-transferase from Methylophilus sp. strain DM11. Ser12 but not Tyr6 is required for enzyme activity. Eur. J. Biochem. 239:410-417.
37. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM. 2005. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 33:D294-D296. http://dx.doi.org/10.1093/nar/gki038.
38. Segata N, Bornigen D, Morgan XC, Huttenhower C. 2013. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat. Commun. 4:2304. http://dx.doi.org/10.1038/ncomms3304.
39. Knief C, Frances L, Vorholt JA. 2010. Competitiveness of diverse Methylobacterium strains in the phyllosphere of Arabidopsis thaliana and identification of representative models, including M. extorquens PA1. Microb. Ecol. 60:440-452. http://dx.doi.org/10.1007/s00248-010-9725-3.
40. 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, Medigue C, Mikhailova N, Nolan M, Woyke T, Stolyar S, Vorholt JA, Vuilleumier S. 2012. Complete genome sequences of six strains of the genus Methylobacterium. J. Bacteriol. 194: 4746-4748. http://dx.doi.org/10.1128/JB.01009-12.
41. Van Aken B, Peres CM, Doty SL, Yoon JM, Schnoor JL. 2004. Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides×nigra DN34). Int. J. Syst. Evol. Microbiol. 54:1191-1196. http://dx.doi.org/10.1099/ijs.0.02796-0.
42. Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B. 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183:214-220. http://dx.doi.org/10.1128/JB.183.1.214-220.2001.
43. Sanders SW, Maxcy RB. 1979. Patterns of cell division, DNA base compositions, and fine structures of some radiation-resistant vegetative bacteria found in food. Appl. Environ. Microbiol. 37:159-168.
44. Valkonen M, Mojzita D, Penttilä M, Benčina M. 2013. Noninvasive high-throughput single-cell analysis of the intracellular pH of Saccharomyces cerevisiae by ratiometric flow cytometry. Appl. Environ. Microbiol. 79:7179-7187. http://dx.doi.org/10.1128/AEM.02515-13.
45. McDonald IR, Doronina NV, Trotsenko YA, McAnulla C, Murrell JC. 2001. Hyphomicrobium chloromethanicum sp. nov. and Methylobacterium chloromethanicum sp. nov., chloromethane-utilizing bacteria isolated from a polluted environment. Int. J. Syst. Evol. Microbiol. 51:119-122. http://dx.doi.org/10.1099/00207713-51-1-119.
46. 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. Proc. Natl. Acad. Sci. U. S. A. 111:2217-2222. http://dx.doi.org/10.1073/pnas.1314561111.