Comparative proteomic analysis of Arthrobacter phenanthrenivorans Sphe3 on phenanthrene, phthalate and glucose

Journal of Proteomics

Volumn 113, Issue , 2015, Pages 73-89

  Vandera, Elpiniki ^a   Samiotaki, Martina ^b   Parapouli, Maria ^a   Panayotou, George ^b   Koukkou, Anna Irini ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

Author keywords

Arthrobacter phenanthrenivorans; Biodegradation; Catabolite repression; Comparative quantitative proteomics; NanoLC MS MS; Phenanthrene

Indexed keywords

AROMATIC COMPOUND; BACTERIAL PROTEIN; GLUCOSE; GLYOXYLIC ACID; PHENANTHRENE; PHTHALIC ACID; PROTOCATECHUIC ACID; SPHE3 PROTEIN; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; PHENANTHRENE DERIVATIVE; PHTHALIC ACID DERIVATIVE; SWEETENING AGENT;

AMINO ACID METABOLISM; ARTHROBACTER; ARTHROBACTER PHENANTHRENIVORANS; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CARBON SOURCE; CATABOLISM; CELL METABOLISM; DEGRADATION; DETOXIFICATION; ENERGY RESOURCE; ENZYME SUBSTRATE; GENE REPRESSION; HYDROXYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN TRANSPORT; PROTEOMICS; QUANTITATIVE ANALYSIS; STRESS; UPREGULATION; BIOSYNTHESIS; COMPARATIVE STUDY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM;

ARTHROBACTER;

ARTHROBACTER; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; PHENANTHRENES; PHTHALIC ACIDS; PROTEOMICS; SWEETENING AGENTS;

EID: 84907993248     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.08.018     Document Type: Article

References (83)

1. Harvey R.G. Polycyclic aromatic hydrocarbons: chemistry and carcinogenicity 1991, Cambridge University Press, Cambridge, UK.
2. Cerniglia C.E. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 1992, 3:351-368.
3. Seo J.S., Keum Y.S., Li Q.X. Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 2009, 6:278-309.
4. Kanaly R.A., Harayama S. Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 2000, 182:2059-2067.
5. Diaz E., Prieto M.A. Bacterial promoters triggering biodegradation of aromatic pollutants. Curr Opin Biotechnol 2000, 11:467-475.
6. Koukkou A.I., Vandera E. Hydrocarbon-degrading soil bacteria: current research. Microbial bioremediation of non-metals 2011, 93-117. Caister Academic Press, Norfolk, UK. A.I. Koukkou (Ed.).
7. Grifoll M., Casellas M., Bayona J.M., Solanas A.M. Isolation and characterization of a fluorene-degrading bacterium: identification of ring oxidation and ring fission products. Appl Environ Microbiol 1992, 58:2910-2917.
8. Samanta S.K., Chakraborti A.K., Jain R.K. Degradation of phenanthrene by different bacteria: evidence for novel transformation sequences involving the formation of 1-naphthol. Appl Microbiol Biotechnol 1999, 53:98-107.
9. Westerberg K., Elväng A.M., Stackebrandt E., Jansson J. Arthrobacter chlorophenolicus sp. nov., a new species capable of degrading high concentrations of 4-chlorophenol. Int J Syst Evol Microbiol 2000, 50:2083-2092.
10. Abraham W.R., Wenderoth D.F., Gläer W. Diversity of biphenyl degraders in a chlorobenzene polluted aquifer. Chemosphere 2005, 58:529-533.
11. Seo J.S., Keum Y.S., Hu Y., Lee S.E., Li O.X. Phenanthrene degradation in Arthrobacter sp. P1-1: initial 1,2-, 3,4- and 9,10-dioxygenation, and meta- and ortho-cleavages of naphthalene-1,2-diol after its formation from naphthalene-1,2-dicarboxylic acid and hydroxyl naphthoic acids. Chemosphere 2006, 65:2388-2394.
12. Joynt J., Bischoff M., Turco R., Konopka A., Nakatsu C.H. Microbial community analysis of soils contaminated with lead, chromium and petroleum hydrocarbons. Microb Ecol 2006, 51:209-219.
13. Kim K.K., Lee K.C., Oh H.M., Kim M.J., Eom M.K., Lee J.S. Arthrobacter defluvii sp. nov., 4-chlorophenol degrading bacteria isolated from sewage. Int J Syst Evol Microbiol 2008, 58:1916-1921.
14. Li Q., Li Y., Zhu X., Cai B. Isolation and characterization of atrazine-degrading Arthrobacter sp. AD26 and use of this strain in bioremediation of contaminated soil. J Environ Sci 2008, 20:1226-1230.
15. Wang Q., Xie S. Isolation and characterization of a high-efficiency soil atrazine-degrading Arthrobacter sp. strain. Int Biodeter Biodegr 2012, 71:61-66.
16. Kallimanis A., Frillingos S., Drainas C., Koukkou A.I. Taxonomic identification, phenanthrene uptake activity and membrane lipid alterations of the PAH degrading Arthrobacter sp. strain Sphe3. Appl Microbiol Biotechnol 2007, 76:709-717.
17. Kallimanis A., Kavakiotis K., Perisynakis A., Spröer C., Pukall R., Drainas C., et al. Arthrobacter phenanthrenivorans sp. nov., to accommodate the phenanthrene degrading bacterium Arthrobacter sp. strain Sphe3. Int J Syst Evol Microbiol 2009, 59:275-279.
18. Kallimanis A., LaButti K.M., Lapidus A., Clum A., Lykidis A., Mavromatis K., et al. Complete genome sequence of Arthrobacter phenanthrenivorans type strain (Sphe3). Stand Genomic Sci 2011, 4:123-130.
19. Vandera E., Kavakiotis K., Kallimanis A., Kyrpides N.C., Drainas C., Koukkou A.I. Heterologous expression and characterization of two 1-hydroxy-2-naphthoic acid dioxygenases from Arthrobacter phenanthrenivorans. Appl Environ Microbiol 2012, 78:621-627.
20. Kim S.I., Choi J.S., Kahng H.Y. A proteomics strategy for the analysis of bacterial biodegradation pathways. OMICS 2007, 11:280-294.
21. Zhao B., Poh C.L. Insights into environmental bioremediation by microorganisms through functional genomics and proteomics. Proteomics 2008, 8:874-881.
22. Kim S.J., Jones R.C., Cha C.J., Kweon O., Edmondson R.D., Cerniglia C.E. Identification of proteins induced by polycyclic aromatic hydrocarbon in Mycobacterium vanbaalenii PYR-1 using two-dimensional polyacrylamide gel electrophoresis and de novo sequencing methods. Proteomics 2004, 4:3899-3908.
23. Bradford M.M. A rapid and sensitive method for the identification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
24. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362.
25. Luber C.A., Cox J., Lauterbach H., Fancke B., Selbach M., Tschopp J., et al. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 2010, 32:279-289.
26. Na K.S., Kuroda A., Takiguchi N., Ikeda T., Ohtake H., Kato J. Isolation and characterization of benzene-tolerant Rhodococcus opacus strains. J Biosci Bioeng 2005, 99:378-382.
27. Treadway S.L., Yanagimachi K.S., Lankenau E., Lessard P.A., Stephanopoulos G., Sinskey A.J. Isolation and characterization of indene bioconversion genes from Rhodococcus strain I24. Appl Microbiol Biotechnol 1999, 51:786-793.
28. Badejo A.C., Badejo A.O., Shin K.H., Chai Y.G. A gene expression study of the activities of aromatic ring-cleavage dioxygenases in Mycobacterium gilvum PYR-GCK to changes in salinity and pH during pyrene degradation. PLoS One 2013, 8:e58066.
29. Krivobok S., Kuony S., Meyer C., Louwagie M., Willison J.C., Jouanneau Y. Identification of pyrene-induced proteins in Mycobacterium sp. 6PY1: evidence for two ring-hydroxylating dioxygenases. J Bacteriol 2003, 185:3828-3841.
30. Kimura N., Kitagawa W., Mori T., Nakashima N., Tamura T., Kamagata Y. Genetic and biochemical characterization of the dioxygenase involved in lateral dioxygenation of dibenzofuran from Rhodococcus opacus strain SAO101. Appl Microbiol Biotechnol 2006, 73:474-484.
31. Iwabuchi T., Harayama S. Biochemical and genetic characterization of trans-2'-carboxybenzalpyruvate hydratase-aldolase from a phenanthrene-degrading Nocardioides strain. J Bacteriol 1998, 180:945-949.
32. Iwabuchi T., Harayama S. Biochemical and genetic characterization of 2-carboxybenzaldehyde dehydrogenase, an enzyme involved in phenanthrene degradation by Nocardioides sp. strain KP7. J Bacteriol 1997, 179:6488-6494.
33. Eaton R.W. Plasmid-encoded phthalate catabolic pathway in Arthrobacter keyseri 12B. J Bacteriol 2001, 183(12):3689-3703.
34. MacLean A.M., MacPherson G., Aneja P., Finan T.M. Characterization of the β-ketoadipate pathway in Sinorhizobium meliloti. Appl Environ Microbiol 2006, 72:5403-5413.
35. Dal S., Trautwein G., Gerischer U. Transcriptional organization of genes for protocatechuate and quinate degradation from Acinetobacter sp. strain ADP1. Appl Environ Microbiol 2005, 71:1025-1034.
36. Harwood C.S., Parales R.E. The β-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 1996, 50:553-590.
37. Kamimura N., Aoyama T., Yoshida R., Takahashi K., Kasai D., Abe T., et al. Characterization of the protocatechuate 4,5-cleavage pathway operon in Comamonas sp. strain E6 and discovery of a novel pathway gene. Appl Environ Microbiol 2010, 76:8093-8101.
38. Noda Y., Nishikawa S., Shiozuka K., Kadokura H., Nakajima H., Yoda K., et al. Molecular cloning of the protocatechuate 4,5dioxygenase genes of Pseudomonas paucimobilis. J Bacteriol 1990, 172:2704-2709.
39. Wattiau P., Bastiaens L., van Herwijnen R., Daal L., Parsons J.R., Renard M.E., et al. Fluorene degradation by Sphingomonas sp. LB126 proceeds through protocatechuic acid: a genetic analysis. Res Microbiol 2001, 152:861-872.
40. Maruyama K., Miwa M., Tsujii N., Nagai T., Tomita N., Harada T., et al. Cloning, sequencing and expression of the gene encoding 4-hydroxy-4-methyl-2-oxoglutarate aldolase from Pseudomonas ochraceae NGJ1. Biosci Biotechnol Biochem 2001, 71:1-15.
41. Kurbatov L., Albrecht D., Herrmann H., Petruschka L. Analysis of the proteome of Pseudomonas putida KT2440 grown on different sources of carbon and energy. Environ Microbiol 2006, 8:466-478.
42. Rojo F. Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 2010, 34:658-684.
43. Dal S., Steiner I., Gerischer U. Multiple operons connected with catabolism of aromatic compounds in Acinetobacter sp. strain ADP1 are under carbon catabolite repression. J Mol Microbiol Biotechnol 2002, 4:389-404.
44. Tomás-Gallardo L., Canosa I., Santero E., Camafeita E., Calvo E., López J.A., et al. Proteomic and transcriptional characterization of aromatic degradation pathways in Rhodoccocus sp. strain TFB. Proteomics 2006, 6:S119-S132.
45. Qi S.W., Chaudhry M.T., Zhang Y., Meng B., Huang Y., Zhao K.X., et al. Comparative proteomes of Corynebacterium glutamicum grown on aromatic compounds revealed novel proteins involved in aromatic degradation and a clear link between aromatic catabolism and gluconeogenesis via fructose-1,6-bisphosphatase. Proteomics 2007, 7:3775-3787.
46. Zhang C., Anderson A.J. Utilization of pyrene and benzoate in Mycobacterium isolate KMS is regulated differentially by catabolic repression. J Basic Microbiol 2013, 53:81-92.
47. Willecke K., Pardee A.B. Fatty acid-requiring mutant of Bacillus subtilis defective in branched chain α-keto acid dehydrogenase. J Biol Chem 1971, 246:5264-5272.
48. Kaneda T. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function and taxonomic significance. Microbiol Rev 1991, 55:288-302.
49. Unell M., Abraham P.E., Shah M., Zhang B., Rückert C., VerBerkmoes N.C., et al. Impact of phenolic substrate and growth temperature on the Arthrobacter chlorophenolicus proteome. J Prot Res 2009, 8:1953-1964.
50. Panda G., Basak T., Tanwer P., Sengupta S., Martins dos Santos V.A.P., Bhatnagar R. Delineating the effect of host environmental signals on a fully virulent strain of Bacillus anthracis using an integrated transcriptomics and proteomics approach. J Prot 2014, 105:242-265.
51. Numa S., Tanabe T. Acetyl-coenzyme A carboxylase and its regulation. New comprehensive biochemistry 1984, vol. 7:1-27. Elsevier Inc., Amsterdam, The Netherlands. A. Neuberger, L.L.M. Van Deenen (Eds.).
52. Fujita Y., Matsuoka H., Hirooka K. Regulation of fatty acid metabolism in bacteria. Mol Microbiol 2007, 66:829-839.
53. Goffin C., Ghuysen J.M. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 1998, 62:1079-1093.
54. Haumann U., Poetsch A. Global proteome of protocatechuate- and glucose-grown Corynebacterium glutamicum reveals multiple physiological differences. J Prot 2012, 75:2649-2656.
55. Fu F., Cheng V.W.T., Wu Y., Tang Y., Weiner J.H., Li L. Comparative proteomic analysis of Staphylococcus warneri SG1 cultured in the presence and absence of butanol. J Proteome Res 2013, 12:4478-4489.
56. Koita K., Rao C.V. Identification and analysis of the putative pentose sugar efflux transporters in Escherichia coli. PLoS One 2012, 7:e43700.
57. Díaz E., Jiménez J.I., Nogales J. Aerobic degradation of aromatic compounds. Curr Opin Biotechnol 2012, 24:1-12.
58. MacLean A.M., Hearty W., Golding G.B., Finan T.M. The LysR-type PcaQ protein regulates expression of a protocatechuate-inducible ABC transport system in Shinorhizobium meliloti. Microbiol 2011, 157:2522-2533.
59. Hara H., Steward G.R., Mohn W.W. Involvement of a novel ABC transporter and monoalkyl phthalate ester hydrolase in Rhodococcus jostii RHA1. Appl Environ Microbiol 2010, 76:1516-1523.
60. Patrauchan M.A., Florizone C., Dosanjh M., Mohn W.W., Davies J., Eltis L.D. Catabolism of benzoate and phthalate in Rhodococcus sp. strain RHA1: redundancies and convergence. J Bacteriol 2005, 187:4050-4063.
61. Marchler-Bauer J., Anderson J.B., Derbyshire M.K., DeWeese-Scott C., Gonzales N.R., Gwadz M., et al. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 2007, 35:D237-D240.
62. Choi K.Y., Kim D., Sul W.J., Chae J.C., Zylstra G.J., Kim Y.M., et al. Molecular and biochemical analysis of phthalate and terephthalate degradation by Rhodococcus sp. strain DK17. FEMS Microbiol Lett 2005, 252:207-213.
63. Van Wely K.H.M., Swaving J., Freudl R., Driessen A.J.M. Translocation of proteins across the cell envelope of Gram-positive bacteria. FEMS Microbiol Rev 2001, 25:437-454.
64. Posey J.E., Shinnick T.M., Quinn F.D. Characterization of the twin-arginine translocation system of Mycobacterium smegmatis. J Bacteriol 2006, 188:1332-1340.
65. Kim Y.E., Hipp M.S., Bracher A., Hayer-Hartl M., Hartl F.U. Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 2013, 82:323-355.
66. Park S.H., Oh K.H., Kim C.K. Adaptive and cross-protective responses of Pseudomonas sp. DJ-12 to several aromatic and other stress shocks. Curr Microbiol 2001, 43:176-181.
67. Domínguez-Cuevas P., González-Pastor J.E., Marqués S., Ramos J.L., deLorenzo V. Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J Biol Chem 2006, 281:11981-11991.
68. De Menezes A., Clipson N., Doyle E. Comparative metatranscriptomics reveals widespread community responses during phenanthrene degradation in soil. Environ Microbiol 2012, 14:2577-2588.
69. Kim S.J., Kweon O., Jones R.C., Edmondson R.D., Cerniglia C.E. Genomic analysis of polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Biodegradation 2008, 19:859-881.
70. Lee S.E., Seo J.S., Keum Y.S., Lee K.J., Li Q.X. Fluoranthene metabolism and associated proteins in Mycobacterium sp. JS14. Proteomics 2007, 7:2059-2069.
71. Badejo A.C., Choi C.W., Badejo A.O., Shin K.H., Hyun J.H., Lee Y.G., et al. A global proteome study of Mycobacterium gilvum PYR-GCK grown on pyrene and glucose reveals the activation of glyoxylate, shikimate and gluconeogenetic pathways through the central carbon metabolism highway. Biodegradation 2013, 24:741-752.
72. Zhang C., Anderson A.J. The gluconeogenic pathway in a soil Mycobacterium isolate with bioremediation ability. Curr Microbiol 2013, 66:122-131.
73. Teufel R., Mascaraque V., Ismail W., Voss M., Perera J., Eisenreich W., et al. Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proc Natl Acad Sci U S A 2010, 107:14390-14395.
74. Navarro-Llorens J.M., Patrauchan M.A., Steward G.R., Davies J.E., Eltis L.D., Mohn W.W. Phenylacetate catabolism in Rhodococcus sp. strain RHA1: a central pathway for degradation of aromatic compounds. J Bacteriol 2005, 187:4497-4504.
75. Ferrández A., Miñambres B., García B., Olivera E.R., Luengo J.M., García J.L., et al. Catabolism of phenylacetic acid in Escherichia coli. J Biol Chem 1998, 273:25974-25986.
76. Olivera E.R., Miñambres B., García B., Muniz C., Moreno M.A., Ferrandez A., et al. Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl-CoA catabolon. Proc Natl Acad Sci 1998, 95:6419-6424.
77. Alonso S., Bartolomé-Martín D., del Álamo M., Díaz E., García J.L., Parera J. Genetic characterization of the styrene lower catabolic pathway of Pseudomonas sp. strain Y2. Gene 2003, 319:71-83.
78. Di Gennaro P., Ferrara S., Ronco I., Galli E., Sello G., Papacchini M., et al. Styrene lower catabolic pathway in Pseudomonas fluorescens ST: identification and characterization of genes for phenylacetic acid degradation. Arch Microbiol 2007, 188:117-125.
79. Shrivastava R., Purohit H., Phale P.S. Metabolism and preferential utilization of phenylacetic acid and 4-hydroxyphenylacetic acid in Pseudomonas putida CSV86. J Bioremed Biodegrad 2011, 2:120.
80. Hamlin J.N.R., Bloodworth R.A.M., Cardona S.T. Regulation of phenylacetic acid degradation genes of Burkholderia cenocepacia K56-2. BMC Microbiol 2009, 9:222.
81. Navarro-Llorens J.M., Drzyzga O., Perera J. Genetic analysis of phenylacetic acid catabolism in Arthrobacter oxydans CECT386. Arch Microbiol 2008, 190:89-100.
82. Shen X.Y., Zhou N.Y., Liu S.J. Degradation and assimilation of aromatic compounds by Corynebacterium glutamicum: another potential for applications for this bacterium?. Appl Microbiol Biotechnol 2012, 95:77-89.
83. Li Y., Wu J., Wang W., Ding P., Feng L. Proteomics analysis of aromatic catabolic pathways in thermophilic Geobacillus thermodnitrificans NG80-2. J Prot 2012, 75:1201-1210.