1887

Abstract

Several bacteria are able to degrade flavonoids either to use them as carbon sources or as a detoxification mechanism. Degradation pathways have been proposed for several bacteria, but the genes responsible are not known. We identified in the genome of the endophyte SmR1 an operon potentially associated with the degradation of aromatic compounds. We show that this operon is involved in naringenin degradation and that its expression is induced by naringenin and chrysin, two closely related flavonoids. Mutation of , the first gene of the operon, and its transcriptional activator, abolished the ability of to degrade naringenin.

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2013-01-01
2020-08-05
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References

  1. Andersen O. M., Markham K. R.. ( 2006;). Flavonoids: Chemistry, Biochemistry and Applications Andersen O. M., Markham K. R.. Boca Raton, FL: CRC Press;
    [Google Scholar]
  2. Arunachalam M., Mohan N., Sugadev R., Chellappan P., Mahadevan A.. ( 2003;). Degradation of (+)-catechin by Acinetobacter calcoaceticus MTC 127. Biochim Biophys Acta1621:261–265 [CrossRef][PubMed]
    [Google Scholar]
  3. Balachandar D., Sandhiya G. S., Sugitha T. C. K., Kumar K.. ( 2006;). Flavonoids and growth hormones influence endophytic colonization and in plant nitrogen fixation by a diazotrophic Serratia sp. in rice. World J Microbiol Biotechnol22:707–712 [CrossRef]
    [Google Scholar]
  4. Baldani J. I., Baldani V. L. D., Seldin L., Döbereiner J.. ( 1986;). Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a root-associated nitrogen-fixing bacterium. Int J Syst Bacteriol36:86–93 [CrossRef]
    [Google Scholar]
  5. Barz W.. ( 1970;). Isolation of rhizosphere bacterium capable of degrading flavonoids. Phytochem9:1745–1749 [CrossRef]
    [Google Scholar]
  6. Bowater L., Fairhurst S. A., Just V. J., Bornemann S.. ( 2004;). Bacillus subtilis YxaG is a novel Fe-containing quercetin 2,3-dioxygenase. FEBS Lett557:45–48 [CrossRef][PubMed]
    [Google Scholar]
  7. Bradford M. M.. ( 1976;). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254 [CrossRef][PubMed]
    [Google Scholar]
  8. Braune A., Gütschow M., Engst W., Blaut M.. ( 2001;). Degradation of quercetin and luteolin by Eubacterium ramulus . Appl Environ Microbiol67:5558–5567 [CrossRef][PubMed]
    [Google Scholar]
  9. Brencic A., Winans S. C.. ( 2005;). Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev69:155–194 [CrossRef][PubMed]
    [Google Scholar]
  10. Coco W. M., Rothmel R. K., Henikoff S., Chakrabarty A. M.. ( 1993;). Nucleotide sequence and initial functional characterization of the clcR gene encoding a LysR family activator of the clcABD chlorocatechol operon in Pseudomonas putida . J Bacteriol175:417–427[PubMed]
    [Google Scholar]
  11. Cook N. C., Samman S.. ( 1996;). Flavonoids – chemistry, metabolism, cardioprotective effects and dietary sources. J Nutr Biochem7:66–76 [CrossRef]
    [Google Scholar]
  12. Das S., Rosazza J. P. N.. ( 2006;). Microbial and enzymatic transformations of flavonoids. J Nat Prod69:499–508 [CrossRef][PubMed]
    [Google Scholar]
  13. Dénarié J., Debellé F., Rosenberg C.. ( 1992;). Signaling and host range variation in nodulation. Annu Rev Microbiol46:497–531 [CrossRef][PubMed]
    [Google Scholar]
  14. Durfee T., Nelson R., Baldwin S., Plunkett G. III, Burland V., Mau B., Petrosino J. F., Qin X., Muzny D. M.. & other authors ( 2008;). The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse. J Bacteriol190:2597–2606 [CrossRef][PubMed]
    [Google Scholar]
  15. Gough C., Galera C., Vasse J., Webster G., Cocking E. C., Dénarié J.. ( 1997;). Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol Plant Microbe Interact10:560–570 [CrossRef][PubMed]
    [Google Scholar]
  16. Hirooka K., Kunikane S., Matsuoka H., Yoshida K. I., Kumamoto K., Tojo S., Fujita Y.. ( 2007;). Dual regulation of the Bacillus subtilis regulon comprising the lmrAB and yxaGH operons and yxaF gene by two transcriptional repressors, LmrA and YxaF, in response to flavonoids. J Bacteriol189:5170–5182 [CrossRef][PubMed]
    [Google Scholar]
  17. Hirooka K., Danjo Y., Hanano Y., Kunikane S., Matsuoka H., Tojo S., Fujita Y.. ( 2009;). Regulation of the Bacillus subtilis divergent yetL and yetM genes by a transcriptional repressor, YetL, in response to flavonoids. J Bacteriol191:3685–3697 [CrossRef][PubMed]
    [Google Scholar]
  18. Hopper W., Mahadevan A.. ( 1997;). Degradation of cathecin by Bradyrhizobium japonicum . Biodeg8:159–165 [CrossRef]
    [Google Scholar]
  19. Jeffrey A. M., Jerina D. M., Self R., Evans W. C.. ( 1972;). The bacterial degradation of flavonoids. Oxidative fission of the A-ring of dihydrogossypetin by a Pseudomonas sp.. Biochem J130:383–390[PubMed]
    [Google Scholar]
  20. Jiménez J. I., Miñambres B., García J. L., Díaz E.. ( 2002;). Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol4:824–841 [CrossRef][PubMed]
    [Google Scholar]
  21. Klassen G., Pedrosa F. O., Souza E. M., Funayama S., Rigo L. U.. ( 1997;). Effect of nitrogen compounds on nitrogenase activity in Herbaspirillum seropedicae SmR1. Can J Microbiol43:887–891 [CrossRef]
    [Google Scholar]
  22. Maddocks S. E., Oyston P. C. F.. ( 2008;). Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology154:3609–3623 [CrossRef][PubMed]
    [Google Scholar]
  23. Miller J. H.. ( 1972;). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  24. Mulligan J. T., Long S. R.. ( 1989;). A family of activator genes regulates expression of Rhizobium meliloti nodulation genes. Genetics122:7–18[PubMed]
    [Google Scholar]
  25. Pedrosa F. O., Monteiro R. A., Wassem R., Cruz L. M., Ayub R. A., Colauto N. B., Fernandez M. A., Fungaro M. H. P., Grisard E. C.. & other authors ( 2011;). Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet7:e1002064 [CrossRef][PubMed]
    [Google Scholar]
  26. Pérez-Pantoja D., De la Iglesia R., Pieper D. H., González B.. ( 2008;). Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol Rev32:736–794 [CrossRef][PubMed]
    [Google Scholar]
  27. Pillai B. V. S., Swarup S.. ( 2002;). Elucidation of the flavonoid catabolism pathway in Pseudomonas putida PML2 by comparative metabolic profiling. Appl Environ Microbiol68:143–151 [CrossRef][PubMed]
    [Google Scholar]
  28. Rao J. R., Cooper J. E.. ( 1994;). Rhizobia catabolize nod gene-inducing flavonoids via C-ring fission mechanisms. J Bacteriol176:5409–5413[PubMed]
    [Google Scholar]
  29. Rao J. R., Cooper J. E.. ( 1995;). Soybean nodulating rhizobia modify nod gene inducers daidzein and genistein to yield aromatic products that can influence gene-inducing activity. Mol Plant Microbe Interact8:855–862 [CrossRef]
    [Google Scholar]
  30. Rao J. R., Sharma N. D., Hamilton J. T. G., Boyd D. R., Cooper J. E.. ( 1991;). Biotransformation of the pentahydroxy flavone quercetin by Rhizobium loti and Bradyrhizobium strains (Lotus). Appl Environ Microbiol57:1563–1565[PubMed]
    [Google Scholar]
  31. Reddy P. M., Rendón-Anaya M., del Río M. D. S., Khandual S.. ( 2007;). Flavonoids as signalling molecules and regulators of root nodule development. Dynamic Soil, Dynamic Plant1:83–94
    [Google Scholar]
  32. Romero-Arroyo C. E., Schell M. A., Gaines G. L. III, Neidle E. L.. ( 1995;). catM encodes a LysR-type transcriptional activator regulating catechol degradation in Acinetobacter calcoaceticus . J Bacteriol177:5891–5898[PubMed]
    [Google Scholar]
  33. Rothmel R. K., Aldrich T. L., Houghton J. E., Coco W. M., Ornston L. N., Chakrabarty A. M.. ( 1990;). Nucleotide sequencing and characterization of Pseudomonas putida catR: a positive regulator of the catBC operon is a member of the LysR family. J Bacteriol172:922–931[PubMed]
    [Google Scholar]
  34. Schneider H., Blaut M.. ( 2000;). Anaerobic degradation of flavonoids by Eubacterium ramulus . Arch Microbiol173:71–75 [CrossRef][PubMed]
    [Google Scholar]
  35. Schoefer L., Mohan R., Schwiertz A., Braune A., Blaut M.. ( 2003;). Anaerobic degradation of flavonoids by Clostridium orbiscindens . Appl Environ Microbiol69:5849–5854 [CrossRef][PubMed]
    [Google Scholar]
  36. Spaink H. P., Okker R. J. H., Wijffelman C. A., Pees E., Lugtenberg B. J. J.. ( 1987;). Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol9:27–39[PubMed][CrossRef]
    [Google Scholar]
  37. Suen W. C., Spain J. C.. ( 1993;). Cloning and characterization of Pseudomonas sp. strain DNT genes for 2,4-dinitrotoluene degradation. J Bacteriol175:1831–1837[PubMed]
    [Google Scholar]
  38. Williams C. A., Grayer R. J.. ( 2004;). Anthocyanins and other flavonoids. Nat Prod Rep21:539–573 [CrossRef][PubMed]
    [Google Scholar]
  39. Winter J., Moore L. H., Dowell V. R. Jr, Bokkenheuser V. D.. ( 1989;). C-ring cleavage of flavonoids by human intestinal bacteria. Appl Environ Microbiol55:1203–1208[PubMed]
    [Google Scholar]
  40. You I. S., Ghosal D., Gunsalus I. C.. ( 1988;). Nucleotide sequence of plasmid NAH7 gene nahR and DNA binding of the nahR product. J Bacteriol170:5409–5415[PubMed]
    [Google Scholar]
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