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Genomic analysis of the aromatic catabolic pathways fromSilicibacter pomeroyi DSS-3

  • Physiology and Metabolism
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Abstract

Genomic analysis of the catabolic potentialities ofSilicibacter pomeroyi DSS-3 against a wide range of natural aromatic compounds and sequence comparisons with the entire genome of this microorganism predicted the existence of at least seven main pathways for the conversion of the aromatic compounds to the intermediates which enter into TCA cycle, that is, the catechol (cat I andcat II genes) and protocatechuate (pca genes) branches of the β-ketoadipate pathway, the phenylacetate pathway (paa genes), the gentisate pathway (gtd genes), the homogentisate pathway (hmg/hppD genes), as well as the homoprotocatechuate pathway (hpc genes). Furthermore, the genes encoding those enzymes involved in the peripheral pathways leading to the β-ketoadipate central pathway were also mapped, i.e., 4-hydroxybenzoate (pob), benzoate (ben), quinate (qui), phenylpropenoid compounds (fcs, ech, vdh, cal, van, acd andact), tyrosine (hpp) and n-phenylalkanoic acids (fad). Evidences showed thatS. pomeroyi DSS-3 have versatile abilities to the catabolism of aromatic compounds either in anaerobic or in aerobic pathway, suggesting such a strain might be a model of heuristic value for the study of the genomic organization, the evolution of genes, as well as the catalytic or transcriptional mechanisms of enzymes for aromatic degradation in marine bacteria. Further, it would provide new insights into the biodegradation of aromatic compounds in marine bacteria and marine environments.

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References

  • Adachi K., Takeda Y., Senoh S., Kita H. (1964). Metabolism ofp-hydroxyphenylacetic acid inPseudomonas ovalis. Biochim. Biophys. Acta, 93: 483–493.

    PubMed  CAS  Google Scholar 

  • Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25: 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  • Aranda-Olmedo I., Tobes R., Manzanera M., Ramos J.L., Marqués S. (2002). Species-specific repetitive extragenic palindromic (REP) sequences inPseudomonas putida. Nucleic Acids Res., 30: 1826–1833.

    Article  PubMed  CAS  Google Scholar 

  • Arias-Barrau E., Olivera E.R., Luengo J.M., Fernandez C, Galan B., Garcia J.L., Diaz E., Minambres B. (2004). The homogentisate pathway: a central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate inPseudomonas putida. J. Bacteriol., 186: 5062–5077.

    Article  PubMed  CAS  Google Scholar 

  • Bayly R.C., Chapman P.J., Dagley S., Di Berardino D. (1980). Purification and some properties of maleylpyruvate hydrolase and fumarylpyruvate hydrolase fromPseudomonas alcaligenes. J. Bacteriol., 143: 70–77.

    PubMed  CAS  Google Scholar 

  • Blakley E.R. (1972). Microbial conversion ofp-hydroxyphenylacetic acid to homogentisic acid. Can. J. Microbiol., 18: 1247–1255.

    PubMed  CAS  Google Scholar 

  • Blakley E.R., Kurz W., Halvorson H., Simpson F.J. (1967). The metabolism of phenylacetic acid by aPseudomonas. Can. J. Microbiol., 13: 147–157.

    PubMed  CAS  Google Scholar 

  • Buchan A., Collier L.S., Neidle E.L., Moran M.A. (2000). Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marineRoseobacter lineage. Appl. Environ. Microbiol., 66: 4662–4672.

    Article  PubMed  CAS  Google Scholar 

  • Chapman P.J., Dagley S. (1962). Oxidation of homogentistic acid by cell-free extracts of a vibrio. J. Gen. Microbiol., 28: 251–256.

    PubMed  CAS  Google Scholar 

  • Clewley J.P. (1995). Macintosh sequence analysis software. DNAStar’s LaserGene. Mol. Biotechnol., 3: 221–224.

    CAS  Google Scholar 

  • Collier L.S., Gaines G.L.I., Neidle E.L. (1998). Regulation of benzoate degradation inAcinetobacter sp. strain ADP1 by BenM, a LysR-type transcriptional activator. J. Bacteriol., 180: 2493–2501.

    PubMed  CAS  Google Scholar 

  • Cowles C.E., Nichols N.N., Harwood C.S. (2000). BenR, a XylS homologue, regulates three different pathways of aromatic acid degradation inPseudomonas putida. J. Bacteriol., 182: 6339–6346.

    Article  PubMed  CAS  Google Scholar 

  • Crawford R.L, Frick T.D. (1977). Rapid spectrophotometric differentiation between glutathione-dependent and glutathioneindependent gentisate and homogentisate pathways. Appl. Environ. Microbiol., 34: 170–174.

    PubMed  CAS  Google Scholar 

  • Denef V.J., Klappenbach J.A., Patrauchan M.A., Florizone C, Rodrigues J.L., Tsoi TV., Verstraete W., Eltis L.D., Tiedje J.M. (2006). Genetic and genomic insights into the role of benzoate-catabolic pathway redundancy inBurkholderia xenovorans LB400. Appl. Environ. Microbiol., 72: 585–595.

    Article  PubMed  CAS  Google Scholar 

  • Dagley S. (1978). Pathways for the utilization of organic substrates. In: Sokatch J.R., Ornston L.N., Eds, The Bacteria, Academic Press, New York, pp. 305–388.

    Google Scholar 

  • Dagley S., Geary P.J., Wood J.M. (1968). The metabolism of protocatechuate byPseudomonas testosteroni. Biochem. J., 109: 559–568.

    PubMed  CAS  Google Scholar 

  • Eaton R.W., Chapman P.J. (1992). Bacterial metabolism of naphthalene: construction and use of recombinant bacteria to study ring cleavage of 1, 2-dihydroxynaphthalene and subsequent reactions. J. Bacterid., 174: 7542–7554.

    CAS  Google Scholar 

  • Ellis L.B.M., Roe D., Wackett L.P. (2006). “The University of Minnesota Biocatalysis/Biodegradation Database: The First Decade,” Nucleic Acids Res., 34: 517–521.

    Article  CAS  Google Scholar 

  • Elsemore D.A., Ornston L.N. (1995). Unusual ancestry of dehydratases associated with quinate catabolism inAcinetobacter calcoaceticus. J. Bacteriol., 177: 5971–5978.

    PubMed  CAS  Google Scholar 

  • Ferrández A., Miñambres B., García B., Olivera E.R., Luengo J.M., García J.L., Díaz E. (1998). Catabolism of phenylacetic acid inEscherichia coli. Characterization of a new aerobic hybrid pathway. J. Biol. Chem., 273: 25974–25986.

    Article  PubMed  Google Scholar 

  • Galibert F., Finan T.M., Long S.R., Puhler A., Abola P., Ampe F, Barloy-Hubler F, Barnett M.J., Becker A., Boistard P., Bothe G., Boutry M., Bowser L., Buhrmester J., Cadieu E., Capela D., Chain P., Cowie A., Davis R.W., Dreano S., Federspiel N.A., Fisher R.F, Gloux S., Godrie T., Goffeau A., Golding B., Gouzy J., Gurjal M., Hernandez-Lucas I., Hong A., Huizar L., Hyman R.W., Jones T., Kahn D., Kahn M.L., Kalman S., Keating D.H., Kiss E., Komp C., Lelaure V., Masuy D., Palm C., Peck M.C., Pohl T.M., Portetelle D., Purnelle B., Ramsperger U., Surzycki R., Thebault P., Vandenbol M., Vorholter F.J., Weidner S., Wells D.H., Wong K., Yeh K.C., Batut J. (2001). The composite genome of the legume symbiontSinorhizobium meliloti. Science, 293: 668–672.

    Article  PubMed  CAS  Google Scholar 

  • Gao X., Tan C.L., Yeo C.C., Poh C.L. (2005). Molecular and biochemical characterization of the xlnD-encoded 3-hydroxybenzoate 6-hydroxylase involved in the degradation of 2,5-xylenol via the gentisate pathway inPseudomonas alcaligenes NCIMB 9867. J. Bacteriol., 187: 7696–7702.

    Article  PubMed  CAS  Google Scholar 

  • Gescher J., Eisenreich W., Worth J., Bacher A., Fuchs G. (2005). Aerobic benzoyl-CoA catabolic pathway inAzoarcus evansii: studies on the non-oxygenolytic ring cleavage enzyme. Mol. Microbiol., 56:1586–1600.

    Article  PubMed  CAS  Google Scholar 

  • Gescher J., Ismail W., Olgeschlager E., Eisenreich W., Worth J., Fuchs G. (2006). Aerobic benzoyl-coenzyme A (CoA) catabolic pathway inAzoarcus evansii: conversion of ring cleavage product by 3,4-dehydroadipyl-CoA semialdehyde dehydrogenase. J. Bacteriol., 188: 2919–2927.

    Article  PubMed  CAS  Google Scholar 

  • Gibson D.T (1980). Microbial Metabolism. In: Hutzinger O., Ed., The Handbook of Environmental Chemistry 2 Part A- Reactions and Processes. Springer Verlag, Berlin, pp. 161–192.

    Google Scholar 

  • Giovannoni S.J., Rappé M.S. (2000). Evolution, diversity and molecular ecology of marine prokaryotes. In: Kirchman D.L., Ed., Microbial Ecology of the Oceans. John Wiley & Sons, Inc., New York, pp. 47–84.

    Google Scholar 

  • Gonzalez J.M., Covert J.S., Whitman W.B., Henriksen J.R., Mayer F., Scharf B., Schmitt R., Buchan A., Fuhrman J.A., Kiene R.P., Moran M.A. (2003).Silicibacter pomeroyi sp. nov. andRoseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int. J. Syst. Evol. Microbiol., 53: 1261–1269.

    Article  PubMed  CAS  Google Scholar 

  • Hagedorn S.R., Chapman P.J. (1985). Glutathione-independent maleylacetoacetate isomerase in Gram-positive bacteria. J. Bacteriol., 163: 803–805.

    PubMed  CAS  Google Scholar 

  • Hagedorn S.R., Bradley G., Chapman P.J. (1985). Glutathione-independent isomerization of maleylpyruvate byBacillus megaterium and other Gram-positive bacteria. J. Bacteriol., 63: 640–647.

    Google Scholar 

  • Harwood C.S., Parales R.E. (1996). The β-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol., 50: 553–590.

    Article  PubMed  CAS  Google Scholar 

  • Houghton J.E., Brown T.M., Appel A.J., Hughes E.J., Ornston L.N. (1995). Discontinuities in the evolution ofPseudomonas putida cat genes. J. Bacteriol., 177: 401–412.

    Article  PubMed  CAS  Google Scholar 

  • Jenkins J.R., Cooper R.A. (1988). Molecular cloning, expression, and analysis of the genes of the homoprotocatechuate catabolic pathway ofEscherichia coli C. J. Bacteriol., 170: 5317–5324.

    PubMed  CAS  Google Scholar 

  • Jimenez J.I., Minambres B., Garcia J.L., Diaz E. (2002). Genomic analysis of the aromatic catabolic pathways fromPseudomonas putida KT2440. Environ. Microbiol., 4: 824–841.

    Article  PubMed  CAS  Google Scholar 

  • Jones D.C., Cooper R.A. (1990). Catabolism of 3-hydroxybenzoate by the gentisate pathway inKlebsiella pneumoniae M5al. Arch. Microbiol., 154: 489–495.

    Article  PubMed  CAS  Google Scholar 

  • Kitagawa W., Suzuki A., Hoaki T, Masai E., Fukuda M. (2001). Multiplicity of aromatic ring hydroxylation dioxygenase genes in a strong PCB degrader,Rhodococcus sp. strain RHA1 demonstrated by denaturing gradient gel electrophoresis. Biosci. Biotechnol. Biochem., 65: 1907–1911.

    Article  PubMed  CAS  Google Scholar 

  • Kiyohara H., Torigoe S., Kaida N., Asaki T., Iida T., Hayashi H., Takizawa N. (1994). Cloning and characterization of a chromosomal gene cluster,pah, that encodes the upper pathway for phenanthrene and naphthalene utilization byPseudomonas putida OUS82. J. Bacteriol., 176: 2439–2443.

    PubMed  CAS  Google Scholar 

  • Krauthammer M., Rzhetsky A., Morozov P., Friedman C. (2000). Using BLAST for identifying gene and protein names in journal articles. Gene., 259: 245–252.

    Article  PubMed  CAS  Google Scholar 

  • Kunita N. (1955). Bacterial oxidation of phenylacetic acid. I I. The pathway through homogentisic acid. Med. J. Osaka Univ., 6: 703–708.

    CAS  Google Scholar 

  • Lack L. (1959). The enzymic oxidation of gentisic acid. Biochim. Biophys. Acta, 34: 117–123.

    Article  PubMed  CAS  Google Scholar 

  • Lack L. (1961). Enzymic cis-trans isomerization of maleylpyruvic acid. J. Biol. Chem., 236: 2835–2840.

    PubMed  CAS  Google Scholar 

  • Laemmli C, Werlen C, van der Meer J.R. (2004). Mutation analysis of the different tfd genes for degradation of chloroaromatic compounds inRalstonia eutropha JMP134. Arch. Microbiol., 181: 112–121.

    Article  PubMed  CAS  Google Scholar 

  • Milcamps A., de Bruijn F.J. (1999). Identification of a novel nutrient-deprivation-inducedSinorhizobium meliloti gene (hmgA) involved in the degradation of tyrosine. Microbiology., 145: 935–947.

    Article  PubMed  CAS  Google Scholar 

  • Mitra A., Kitamura Y., Gasson M.J., Narbad A., Parr A.J., Payne J., Rhodes M.J., Sewter C, Walton N.J. (1999). 4-Hydroxycinnamoyl-CoA hydratase/lyase (HCHL) — n enzyme of phenylpropanoid chain cleavage fromPseudomonas. Arch. Biochem. Biophys., 365: 10–16.

    Article  PubMed  CAS  Google Scholar 

  • Mohamed M.E., Ismail W., Heider J., Fuchs G. (2002). Aerobic metabolism of phenylacetic acids inAzoarcus evansii. Arch. Microbiol., 178: 180–192.

    Article  CAS  Google Scholar 

  • Moran M.A., Buchan A., Gonzalez J.M., Heidelberg J.F., Whitman W.B., Kiene R.P., Henriksen J.R., King G.M., Belas R., Fuqua C, Brinkac L., Lewis M., Johri S., Weaver B., Pai G., Eisen J.A., Rahe E., Sheldon W.M., Ye W., Miller T.R., Carlton J., Rasko D.A., Paulsen I.T., Ren Q., Daugherty S.C., Deboy R.T., Dodson R.J., Durkin A.S., Madupu R., Nelson W.C., Sullivan S.A., Rosovitz M.J., Haft D.H., Selengut J., Ward N. (2004). Genome sequence ofSilicibacter pomeroyi reveals adaptations to the marine environment. Nature., 432: 910–913.

    Article  PubMed  CAS  Google Scholar 

  • Nichols N.N., Harwood C.S. (1997). PcaK, a high-affinity permease for the aromatic compounds 4-hydroxybenzoate and protocatechuate fromPseudomonas putida. J. Bacteriol., 179: 5056–5061.

    PubMed  CAS  Google Scholar 

  • Olivera E.R., Carnicero D., Garcia B., Minambres B., Moreno M.A., Canedo L, Dirusso C.C., Luengo J.M. (2001). Two different pathways are involved in the β-oxidation of n-alkanoic and nphenylalkanoic acids inPseudomonas putida U: genetic studies and biotechnological applications. Mol. Microbiol., 39: 863–874.

    Article  PubMed  CAS  Google Scholar 

  • Overhage J., Priefert H., Steinbüchel A. (1999). Biochemical and genetic analyses of ferulic acid catabolism inPseudomonas sp. strain HR199. Appl. Environ. Microbiol., 65: 4837–4847.

    PubMed  CAS  Google Scholar 

  • Patrauchan M.A., Florizone C, Dosanjh M., Mohn W.W., Davies J., Eltis L.D. (2005). Catabolism of benzoate and phthalate inRhodococcus sp. strain RHA1: redundancies and convergence. J. Bacteriol., 187: 4050–4063.

    Article  PubMed  CAS  Google Scholar 

  • Parrot S., Jones S., Cooper R.A. (1987). 2-Phenylethylamine catabolism byEscherichia coli K12. J. Gen. Microbiol., 133: 347–351.

    Google Scholar 

  • Poh C.L., Bayly R.C. (1980). Evidence for isofunctional enzymes used in m-cresol and 2,5-xylenol degradation via the gentisate pathway inPseudomonas alcaligenes. J. Bacteriol., 143: 59–69.

    PubMed  CAS  Google Scholar 

  • Priefert H., Rabenhorst J., Steinbüchel A. (1997). Molecular characterization of genes ofPseudomonas sp. strain HR199 involved in bioconversion of vanillin to protocatechuate. J. Bacteriol., 179: 2595–2607.

    PubMed  CAS  Google Scholar 

  • Priefert H., Rabenhorst J., Steinbüchel A. (2001). Biotechnological production of vanillin. Appl. Microbiol. Biotechnol., 56: 296–314.

    Article  PubMed  CAS  Google Scholar 

  • Prieto M.A., Díaz E., García J.L. (1996). Molecular characterization of the 4-hydroxyphenylacetate catabolic pathway ofEscherichia coli W: engineering a mobile aromatic degradative cluster. J. Bacteriol., 178: 111–120.

    Article  PubMed  CAS  Google Scholar 

  • Robson N.D., Parrott S., Cooper R.A. (1996).In vitro formation of a catabolic plasmid carryingKlebsiella pneumoniae DNA that allows growth ofEscherichia coli K-12 on 3-hydroxybenzoate. Microbiology, 142: 2115–2120.

    Article  PubMed  CAS  Google Scholar 

  • Roper D.I., Fawcett T., Cooper R.A. (1993). TheEscherichia coli C homoprotocatechuate degradative operon:hpc gene order, direction of transcription and control of expression. Mol. Gen. Genet., 237: 241–250.

    Article  PubMed  CAS  Google Scholar 

  • Segura A., Bünz P.V., D’Argenio D.A., Ornston L.N. (1999). Genetic analysis of a chromosomal region containingvanA andvanB genes required for conversion of either ferulate or vanillate to protocatechuate inAcinetobacter. J. Bacteriol., 181: 3494–3504.

    PubMed  CAS  Google Scholar 

  • Shen X.H., Jiang C.Y., Huang Y., Liu Z.P., Liu S.J. (2005). Functional identification of novel genes involved in the glutathione-independent gentisate pathway inCorynebacterium glutamicum. Appl. Environ. Microbiol., 71: 3442–3452.

    Article  PubMed  CAS  Google Scholar 

  • Song J., Jensen R.A. (1996). PhhR, a divergently transcribed activator of the phenylalanine hydroxylase gene cluster ofPseudomonas aeruginosa. Mol. Microbiol., 22: 497–507.

    Article  PubMed  CAS  Google Scholar 

  • Sparnins V.L., Chapman P.J. (1976). Catabolism of L-tyrosine by the homoprotocatechuate pathway in Gram-positive bacteria J. Bacteriol., 127: 362–366.

    PubMed  CAS  Google Scholar 

  • Takami H., Nakasone K., Takaki Y., Maeno G., Sasaki R., Masui N., Fuji F., Hirama C, Nakamura Y, Ogasawara N., Kuhara S., Horikoshi K. (2000). Complete genome sequence of the alkaliphilic bacteriumBacillus halodurans and genomic sequence comparison withBacillus subtilis. Nucleic Acids Res., 28: 4317–4331.

    Article  PubMed  CAS  Google Scholar 

  • Tobes R., Ramos J.L. (2005). REP code: defining bacterial identity in extragenic space. Environ. Microbiol., 7: 225–228.

    Article  PubMed  CAS  Google Scholar 

  • Venturi V., Zennaro F, Degrassi G., Okeke B.C., Bruschi C.V. (1998). Genetics of ferulic acid bioconversion to protocatechuic acid in plant-growth-promotingPseudomonas putida WCS358. Microbiology, 144: 965–973.

    Article  PubMed  CAS  Google Scholar 

  • Zhou N.Y., Fuenmayor S.L., Williams P.A. (2001).nag genes of Ralstonia (formerlyPseudomonas) sp. strain U2 encoding enzymes for gentisate catabolism. J. Bacteriol., 183: 700–708.

    Article  PubMed  CAS  Google Scholar 

  • Zhang R., Zhang C.T. (2005). Genomic islands in theCorynebacterium efficiens genome. Appl. Environ. Microbiol., 71: 3126–3130.

    Article  PubMed  CAS  Google Scholar 

  • Zhuang Z., Song F., Takami H., Dunaway-Mariano D. (2004). The BH1999 protein ofBacillus halodurans C-125 is gentisyl-coenzyme A thioesterase. J. Bacteriol., 186: 393–399.

    Article  PubMed  CAS  Google Scholar 

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Yan, D., Kang, J. & Liu, DQ. Genomic analysis of the aromatic catabolic pathways fromSilicibacter pomeroyi DSS-3. Ann. Microbiol. 59, 789–800 (2009). https://doi.org/10.1007/BF03179225

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