Whole-Genome Analysis of the Methyl tert -Butyl Ether-Degrading Beta-Proteobacterium Methylibium petroleiphilum PM1

Journal of Bacteriology - Tập 189 Số 5 - Trang 1931-1945 - 2007
Staci R. Kane1, Anu Chakicherla1, Patrick Chain2,1, Radomir Schmidt3, Maria Shin1, Tina C. Legler1, Kate M. Scow3, Frank W. Larimer4,2, Susan Lucas2, Paul M. Richardson2, Krassimira R. Hristova3
1Lawrence Livermore National Laboratory, Livermore, California
2Joint Genome Institute Production Genomics Facility, Walnut Creek, California
3Department of Land, Air, and Water Resources, University of California, Davis, California
4Genome Analysis Group, Oak Ridge National Laboratory, Oak Ridge, Tennessee

Tóm tắt

ABSTRACT Methylibium petroleiphilum PM1 is a methylotroph distinguished by its ability to completely metabolize the fuel oxygenate methyl tert -butyl ether (MTBE). Strain PM1 also degrades aromatic (benzene, toluene, and xylene) and straight-chain (C 5 to C 12 ) hydrocarbons present in petroleum products. Whole-genome analysis of PM1 revealed an ∼4-Mb circular chromosome and an ∼600-kb megaplasmid, containing 3,831 and 646 genes, respectively. Aromatic hydrocarbon and alkane degradation, metal resistance, and methylotrophy are encoded on the chromosome. The megaplasmid contains an unusual t-RNA island, numerous insertion sequences, and large repeated elements, including a 40-kb region also present on the chromosome and a 29-kb tandem repeat encoding phosphonate transport and cobalamin biosynthesis. The megaplasmid also codes for alkane degradation and was shown to play an essential role in MTBE degradation through plasmid-curing experiments. Discrepancies between the insertion sequence element distribution patterns, the distributions of best BLASTP hits among major phylogenetic groups, and the G+C contents of the chromosome (69.2%) and plasmid (66%), together with comparative genome hybridization experiments, suggest that the plasmid was recently acquired and apparently carries the genetic information responsible for PM1's ability to degrade MTBE. Comparative genomic hybridization analysis with two PM1-like MTBE-degrading environmental isolates (∼99% identical 16S rRNA gene sequences) showed that the plasmid was highly conserved (ca. 99% identical), whereas the chromosomes were too diverse to conduct resequencing analysis. PM1's genome sequence provides a foundation for investigating MTBE biodegradation and exploring the genetic regulation of multiple biodegradation pathways in M. petroleiphilum and other MTBE-degrading beta-proteobacteria.

Từ khóa


Tài liệu tham khảo

Afolabi, P. R., F. Mohammed, K. Amaratunga, O. Majekodunmi, S. L. Dales, R. Gill, D. Thompson, J. B. Cooper, S. P. Wood, P. M. Goodwin, and C. Anthony. 2001. Site-directed mutagenesis and X-ray crystallography of the PQQ-containing quinoprotein methanol dehydrogenase and its electron acceptor, cytochrome cL. Biochemistry 40 : 9799-9809.

Asperger, O., A. Naumann, and H.-P. Kleber. 1984. Inducibility of cytochrome P-450 in Acinetobacter calcoaceticus by n-alkanes. Appl. Microbiol. Biotechnol. 19 : 3948-4403.

Atkinson, R. 1995. Gas phase tropospheric chemistry of organic compounds. Environ. Sci. Technol. 4 : 65-89.

Atomi, H. 2002. Microbial enzymes involved in carbon dioxide fixation. J. Biosci. Bioeng. 94 : 497-505.

Ausubel F. M. R. Brent R. E. Kingston D. D. Moore J. G. Seidman J. A. Smith and K. Stuhl. 1987. Current protocols in molecular biology. Wiley New York NY.

Backert, S., and T. F. Meyer. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9 : 207-217.

10.1128/AEM.68.1.289-296.2002

Braun, V., and M. Braun. 2002. Iron transport and signaling in Escherichia coli. FEBS Lett. 529 : 78-85.

Bruns, M. A., J. R. Hanson, J. Mefford, and K. M. Scow. 2001. Isolate PM1 populations are dominant and novel methyl tert-butyl ether-degrading bacteria in compost biofilter enrichments. Environ. Microbiol. 3 : 220-225.

10.1128/AEM.66.5.1826-1833.2000

10.1128/jb.178.21.6327-6337.1996

10.1128/AEM.70.4.2211-2219.2004

Cervantes, C., and F. Gutierrez-Corona. 1994. Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol. Rev. 14 : 121-137.

10.1128/JB.185.9.2759-2773.2003

10.1128/JB.183.22.6551-6557.2001

10.1128/jb.170.2.781-789.1988

Chistoserdova, L., and M. E. Lidstrom. 1997. Molecular and mutational analysis of a DNA region separating two methylotrophy gene clusters in Methylobacterium extorquens AM1. Microbiology 143 : 1729-1736.

Davis-Hoover, W. J., S. A. Stavnes, J. J. Fleischman, S. C. Hunt, J. Goetz, M. Kemper, M. Roulier, K. Hristova, K. Scow, K. Knutson, W. R. Mahaffey, and D. J. Slomczynski. 2003. BTEX/MTBE bioremediation: bionets containing Isolite, PM1, SOS or air, p. E-25. In V. S. Magar and M. E. Kelley (ed.), Proceedings of the Seventh International In Situ and On-Site Bioremediation Symposium. Battelle Press, Columbus, OH.

Abstr. Am. Chem. Soc. 2000 219

Deeb, R. A., H.-Y. Hu, J. R. Hanson, K. M. Scow, and L. Alvarez-Cohen. 2001. Substrate interactions in BTEX and MTBE mixtures by an MTBE-degrading isolate. Environ. Sci. Technol. 35 : 312-317.

De Marco, P., C. Pachecoa, A. Figueiredoa, and P. Moradas-Ferreira. 2004. Novel pollutant-resistant methylotrophic bacteria for use in bioremediation. FEMS Lett. 234 : 75-80.

10.1128/AEM.64.7.2710-2715.1998

Elango, N., R. Radhakrishnan, W. A. Froland, B. J. Wallar, C. A. Earhart, J. D. Lipscomb, and D. H. Ohlendorf. 1997. Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci. 6 : 556-568.

Reference deleted.

10.1101/gr.8.3.186

10.1101/gr.8.3.175

Fayolle, F., J.-P. Vandecasteele, and F. Monot. 2001. Microbial degradation and fate in the environment of methyl tert-butyl ether and related fuel oxygenates. Appl. Microbiol. Biotechnol. 56 : 339-349.

Felsenstein J. 2002. PHYLIP (Phylogeny Inference Package) version 3.6a3. Department of Genome Sciences University of Washington Seattle.

Fishman, A., Y. Tao, and T. K. Wood. 2004. Physiological relevance of successive hydroxylations of toluene para-monooxygenase of Ralstonia pickettii PKO1. Biocat. Biotrans. 22 : 283-289.

10.1128/AEM.68.6.2754-2762.2002

Fujii, T., T. Narikawa, K. Takeda, and J. Kato. 2004. Biotransformation of various alkanes using the Escherichia coli expressing an alkane hydroxylase system from Gordonia sp. TF6. Biosci. Biotechnol. Biochem. 68 : 2171-2177.

10.1101/gr.8.3.195

10.1128/AEM.67.11.4992-4998.2001

10.1128/AEM.65.11.4788-4792.1999

Hara, A., S. H. Baik, K. Syutsubo, N. Misawa, T. H. Smits, J. B. van Beilen, and S. Harayama. 2004. Cloning and functional analysis of alkB genes in Alcanivorax borkumensis SK2. Environ. Microbiol. 6 : 191-197.

10.1128/AEM.67.12.5601-5607.2001

10.1128/JB.180.22.6031-6038.1998

10.1128/AEM.69.5.2616-2623.2003

10.1128/AEM.67.11.5154-5160.2001

Hugler, H., H. Huber, K. O. Stetter, and G. Fuchs. 2003. Autotrophic CO2 fixation pathways in archaea (Crenoarchaeota). Arch. Microbiol. 179 : 160-173.

Jeanmougin, F., J. D. Thompson, M. Gouy, D. G. Higgins, and T. J. Gibson. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23 : 403-405.

Jimenez, J. I., B. Minambres, J. L. Garcia, and E. Diaz. 2002. Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ. Microbiol. 4 : 824-841.

10.1128/JB.182.5.1232-1242.2000

10.1128/JB.187.13.4607-4614.2005

Kamerbeek, N. M., M. J. H. Moonen, J. G. M. van der Ven, W. J. H. van Berkel, M. W. Fraaije, and D. B. Janssen. 2001. 4-Hydroxyacetophenone monooxygenase from Pseudomonas fluorescens ACB. A novel flavoprotein catalyzing Baeyer-Villiger oxidation of aromatic compounds. Eur. J. Biochem. 268 : 2547-2557.

10.1128/AEM.67.12.5824-5829.2001

Kane, S. R., T. C. Legler, L. M. Balser, and K. T. O'Reilly. 2003. Aerobic biodegradation of MTBE by aquifer bacteria from LUFT sites, p. E-12. In V. S. Magar and M. E. Kelley (ed.), Proceedings of the Seventh International In Situ and On-Site Bioremediation Symposium. Battelle Press, Columbus, OH.

Kitiyama, A., E. Suzuki, Y. Kawakami, and T. Nagamune. 1996. Gene organization and low regiospecificity in aromatic-ring hydroxylation of a benzene monooxygenase of Pseudomonas aeruginosa JI104. J. Ferment. Bioeng. 82 : 421-425.

10.1128/JB.181.17.5317-5329.1999

10.1128/JB.185.24.7120-7128.2003

10.1128/AEM.67.5.2197-2201.2001

Lopes Ferreira, N., D. Labbe, F. Monot, F. Fayolle-Guichard, and C. W. Greer. 2006. Genes involved in the methyl tert-butyl ether (MTBE) pathway of Mycobacterium austroafricanum IFP 2012. Microbiology 152 : 1361-1374.

Malito, E., A. Alfieri, M. W. Fraaije, and A. Mattevi. 2004. Crystal structure of a Baeyer-Villiger monooxygenase. Proc. Natl. Acad. Sci. USA 101 : 13157-13162.

Mergeay, M., S. Monchy, T. Vallaeys, V. Auquier, A. Benotmane, P. Bertin, S. Taghavi, J. Dunn, D. van der Lelie, and R. Wattiez. 2003. Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol. Rev. 27 : 385-410.

Moreels, D., L. Bastiaens, F. Ollevier, R. Merckx, L. Diels, and D. Springael. 2004. Evaluation of the intrinsic methyl tert-butyl ether (MTBE) biodegradation potential of hydrocarbon contaminated subsurface soils in batch microcosm systems. FEMS Microbiol. Ecol. 49 : 121-128.

10.1128/aem.60.7.2661-2665.1994

Nakatsu, C. H., K. R. Hristova, S. Hanada, X.-Y. Meng, J. R. Hanson, K. M. Scow, and Y. Kamagata. 2006. Methylibium petroleiphilum PM1 gen. nov., sp. nov., a new methyl tert-butyl ether (MTBE) degrading methylotroph belonging to the beta-subclass of the proteobacteria. Int. J. Syst. Evol. Microbiol. 56 : 983-989.

Oh, J.-I., and B. Bowien. 1998. Structural analysis of the fds operon encoding the NAD+-linked formate dehydrogenase of Ralstonia eutropha. J. Biol. Chem. 273 : 26349-26360.

Piveteau, P., F. Fayolle, J.-P. Vandecasteele, and F. Monot. 2001. Biodegradation of t-butyl alcohol and related xenobiotics by a methylotrophic bacterial isolate. Appl. Microbiol. Technol. 55 : 369-373.

10.1074/jbc.M305837200

10.1128/AEM.00080-06

Rosen, B. P. 2002. Biochemistry of arsenic detoxification. FEBS Lett. 529 : 86-92.

Ryan, D., and E. Colleran. 2002. Arsenic resistance in the IncH12 plasmids. Plasmids 47 : 234-240.

10.1271/bbb.58.2128

10.1128/aem.60.7.2593-2596.1994

10.1128/jb.174.3.711-724.1992

Smith, A. E., K. Hristova, I. Wood, D. M. Mackay, E. Lory, D. Lorenzana, and K. M. Scow. 2005. Comparison of biostimulation versus bioaugmentation with bacterial strain PM1 for treatment of groundwater contaminated with methyl tertiary butyl ether (MTBE). Environ. Health Prospect. 113 : 317-332.

10.1128/AEM.69.2.796-804.2003

10.1128/AEM.70.8.4544-4550.2004

10.1128/AEM.69.12.7385-7394.2003

10.1128/AEM.68.11.5265-5273.2002

10.1128/JB.184.6.1733-1742.2002

Stavnes, S. A., J. Fleischman, J. Goetz, K. Hristova, S. Hunt, M. Kemper, K. Knutson, W. Mahaffee, M. Roulier, K. Scow, D. J. Slomczynski, and W. J. Davis-Hoover. 2002. MTBE bioremediation with BioNets containing Isolite, PM1, SOS or air, p. 2B-66. In A. R. Gavaskar and A. S. C. Chen (ed.), Proceedings of the Third International Conference of Chlorinated and Recalcitrant Compounds. Battelle Press, Columbus, OH.

10.1128/aem.63.11.4216-4222.1997

10.1128/JB.183.5.1819-1823.2001

10.1128/AEM.70.7.3814-3820.2004

10.1093/nar/28.1.33

Trevors, J. T. 1986. Plasmid curing in bacteria. FEMS Microbiol. Rev. 32 : 149-157.

van Beilen, J. B., S. Panke, S. Lucchini, A. G. Franchini, M. Rothlisberger, and B. Witholt. 2001. Analysis of Pseudomonas putida alkane degradation gene clusters and flanking insertion sequences: evolution and regulation of the alk genes. Microbiology 147 : 1621-1630.

10.1128/JB.184.6.1722-1732.2002

10.1128/JB.186.14.4730-4739.2004

Wilson, R. D., D. M. Mackay, and K. M. Scow. 2002. In situ MTBE biodegradation supported by diffusive oxygen release. Environ. Sci. Technol. 36 : 190-199.

Zhulin, I. B. 2001. The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv. Microb. Physiol. 45 : 157-198.