The involvement of bacterial aromatic ring-hydroxylating dioxygenases (ARHDs) in the degradation of aromatic pollutants, such as polychlorinated biphenyls (PCBs), has been well studied. However, there is considerable speculation as to the origin of this ability. One hypothesis is centered on a connection between the ability to degrade aromatic pollutants and the necessity of soil bacteria to cope with and/or utilize secondary plant metabolites (SPMs). To investigate this connection, we researched the involvement of biphenyl 2,3-dioxygenase (BPDO), an ARHD essential for the degradation of PCBs, in the metabolism of SPMs in the soil bacterium Pseudomonas alcaliphila JAB1, a versatile degrader of PCBs. We demonstrated the ability of the strain JAB1 to transform a variety of SPMs, namely the flavonoids apigenin, flavone, flavanone, naringenin, fisetin, quercetin, morin, and catechin, caffeic acid, trans-cinnamic acid, and the monoterpenes (S)-limonene and (R)-carvone. Of those, the transformation of flavone, flavanone, and (S)-limonene was conditioned by the activity of JAB1-borne BPDO and thus was researched in more detail, and we found evidence for the limonene monooxygenase activity of the BPDO. Furthermore, the bphA gene in the strain JAB1 was demonstrated to be induced by a wide range of SPMs, with monoterpenes being the strongest inducers of the SPMs tested. Thus, our findings contribute to the growing body of evidence that ARHDs not only play a role in the catabolism of aromatic pollutants, but also of natural plant-derived aromatics, and this study supports the hypothesis that ARHDs participate in ecological processes mediated by SPMs.

Department of Biochemistry and Microbiology Faculty of Food and Biochemical Technology University of Chemistry and Technology Prague Czechia

Faculty of Science Institute for Environmental Studies Charles University Prague Czechia

Institute of Microbiology Academy of Sciences of the Czech Republic Prague Czechia

Zobrazit více v PubMed

Agullo L., Romero-Silva M. J., Domenech M., Seeger M. (2017). p-cymene promotes its catabolism through the p-cymene and the p-cumate pathways, activates a stress response and reduces the biofilm formation in Burkholderia xenovorans LB400. PLoS One 12:e0169544. 10.1371/journal.pone.0169544, PMID: PubMed DOI PMC

Aoki H., Kimura T., Habe H., Yamane H., Kodama T., Omori T. (1996). Cloning, nucleotide sequence, and characterization of the genes encoding enzymes involved in the degradation of cumene to 2-hydroxy-6-oxo-7-methylocta-2,4-dienoic acid in Pseudomonas fluorescens IP01. J. Ferment. Bioeng. 81, 187–196. 10.1016/0922-338X(96)82207-0 DOI

Baldwin B. R., Mesarch M. B., Nies L. (2000). Broad substrate specificity of naphthalene- and biphenyl-utilizing bacteria. Appl. Microbiol. Biotechnol. 53, 748–753. 10.1007/s002539900300, PMID: PubMed DOI

Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300. 10.1111/j.2517-6161.1995.tb02031.x DOI

Böttger A., Vothknecht U., Bolle C., Wolf A. (eds.) (2018). “Plant Secondary Metabolites and Their General Function in Plants,” in Lessons on Caffeine, Cannabis & Co: Plant-derived Drugs and Their Interaction With Human Receptors. (Cham: Springer International Publishing; ), 3–17.

Cadwallader K. R., Braddock R. J., Parish M. E., Higgins D. P. (1989). Bioconversion of (+)-limonene by Pseudomonas gladioli. J. Food Sci. 54, 1241–1245. 10.1111/j.1365-2621.1989.tb05964.x DOI

Cesco S., Mimmo T., Tonon G., Tomasi N., Pinton R., Terzano R., et al. . (2012). Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol. Fertil. Soils 48, 123–149. 10.1007/s00374-011-0653-2 DOI

Cesco S., Neumann G., Tomasi N., Pinton R., Weisskopf L. (2010). Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329, 1–25. 10.1007/s11104-009-0266-9 DOI

Cheong T. K., Oriel P. J. (2000). Cloning and expression of the limonene hydroxylase of Bacillus stearothermophilus BR388 and utilization in two-phase limonene conversions. Appl. Biochem. Biotechnol. 84, 903–915. 10.1385/abab:84-86:1-9:903, PMID: PubMed DOI

Chun H.-K., Ohnishi Y., Shindo K., Misawa N., Furukawa K., Horinouchi S. (2003). Biotransformation of flavone and flavanone by Streptomyces lividans cells carrying shuffled biphenyl dioxygenase genes. J. Mol. Catal. B Enzym. 21, 113–121. 10.1016/S1381-1177(02)00085-1 DOI

Chung S.-Y., Maeda M., Song E., Horikoshij K., Kudo T. (1994). A gram-positive polychlorinated biphenyl-degrading bacterium, Rhodococcus erythropolis strain TA421, isolated from a termite ecosystem. Biosci. Biotechnol. Biochem. 58, 2111–2113. 10.1271/bbb.58.2111 DOI

Dakora F. D., Phillips D. A. (1996). Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Physiol. Mol. Plant Pathol. 49, 1–20. 10.1006/pmpp.1996.0035 DOI

Dennis P. G., Miller A. J., Hirsch P. R. (2010). Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol. Ecol. 72, 313–327. 10.1111/j.1574-6941.2010.00860.x, PMID: PubMed DOI

Donnelly P. K., Hegde R. S., Fletcher J. S. (1994). Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28, 981–988. 10.1016/0045-6535(94)90014-0 DOI

Duetz W. A., Fjallman A. H., Ren S., Jourdat C., Witholt B. (2001). Biotransformation of D-limonene to (+) trans-carveol by toluene-grown Rhodococcus opacus PWD4 cells. Appl. Environ. Microbiol. 67, 2829–2832. 10.1128/AEM.67.6.2829-2832.2001, PMID: PubMed DOI PMC

Durante-Rodríguez G., Gómez-Álvarez H., Nogales J., Carmona M., Díaz E. (2018). “One-Component Systems That Regulate the Expression of Degradation Pathways for Aromatic Compounds,” in Cellular Ecophysiology of Microbe: Hydrocarbon and Lipid Interactions. ed. Krell T. (Cham: Springer International Publishing; ), 137–175.

Eaton R. W. (1996). p-Cumate catabolic pathway in Pseudomonas putida Fl: cloning and characterization of DNA carrying the cmt operon. J. Bacteriol. 178, 1351–1362. 10.1128/JB.178.5.1351-1362.1996, PMID: PubMed DOI PMC

Eltis L. D., Bolin J. T. (1996). Evolutionary relationships among extradiol dioxygenases. J. Bacteriol. 178, 5930–5937. 10.1128/JB.178.20.5930-5937.1996, PMID: PubMed DOI PMC

Falcone Ferreyra M. L., Rius S. P., Casati P. (2012). Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front. Plant Sci. 3:222. 10.3389/fpls.2012.00222, PMID: PubMed DOI PMC

Focht D. D. (1995). Strategies for the improvement of aerobic metabolism of polychlorinated biphenyls. Curr. Opin. Biotechnol. 6, 341–346. 10.1016/0958-1669(95)80057-3 DOI

Fraraccio S., Strejcek M., Dolinova I., Macek T., Uhlik O. (2017). Secondary compound hypothesis revisited: selected plant secondary metabolites promote bacterial degradation of cis-1,2-dichloroethylene (cDCE). Sci. Rep. 7:11. 10.1038/s41598-017-07760-1, PMID: PubMed DOI PMC

Furukawa K., Fujihara H. (2008). Microbial degradation of polychlorinated biphenyls: biochemical and molecular features. J. Biosci. Bioeng. 105, 433–449. 10.1263/jbb.105.433, PMID: PubMed DOI

Furukawa K., Suenaga H., Goto M. (2004). Biphenyl dioxygenases: functional versatilities and directed evolution. J. Bacteriol. 186, 5189–5196. 10.1128/JB.186.16.5189-5196.2004, PMID: PubMed DOI PMC

Ganger M. T., Dietz G. D., Ewing S. J. (2017). A common base method for analysis of qPCR data and the application of simple blocking in qPCR experiments. BMC Bioinform. 18:534. 10.1186/s12859-017-1949-5, PMID: PubMed DOI PMC

Garrido-Sanz D., Sansegundo-Lobato P., Redondo-Nieto M., Suman J., Cajthaml T., Blanco-Romero E., et al. . (2020). Analysis of the biodegradative and adaptive potential of the novel polychlorinated biphenyl degrader Rhodococcus sp. WAY2 revealed by its complete genome sequence. Microb. Genom. 6:e000363. 10.1099/mgen.0.000363, PMID: PubMed DOI PMC

Gilbert E. S., Crowley D. E. (1997). Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl. Environ. Microbiol. 63, 1933–1938. 10.1128/AEM.63.5.1933-1938.1997, PMID: PubMed DOI PMC

Gilbert E. S., Crowley D. E. (1998). Repeated application of carvone-induced bacteria to enhance biodegradation of polychlorinated biphenyls in soil. Appl. Microbiol. Biotechnol. 50, 489–494. 10.1007/s002530051325, PMID: PubMed DOI

González-Pasayo R., Martínez-Romero E. (2000). Multiresistance genes of Rhizobium etli CFN42. Mol. Plant-Microbe Interact. 13, 572–577. 10.1094/MPMI.2000.13.5.572, PMID: PubMed DOI

Górniak I., Bartoszewski R., Króliczewski J. (2019). Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem. Rev. 18, 241–272. 10.1007/s11101-018-9591-z DOI

Groeneveld M., van Beek H. L., Duetz W. A., Fraaije M. W. (2016). Identification of a novel oxygenase capable of regiospecific hydroxylation of D-limonene into (+)-trans-carveol. Tetrahedron 72, 7263–7267. 10.1016/j.tet.2015.12.061 DOI

Han J., Kim S.-Y., Jung J., Lim Y., Ahn J.-H., Kim S.-I., et al. . (2005). Epoxide formation on the aromatic B-ring of flavanone by biphenyl dioxygenase of Pseudomonas pseudoalcaligenes KF707. J. Appl. Environ. Microbiol. 71, 5354–5361. 10.1128/AEM.71.9.5354-5361.2005, PMID: PubMed DOI PMC

Harborne J. B., Williams C. A. (2000). Advances in flavonoid research since 1992. Phytochemistry 55, 481–504. 10.1016/S0031-9422(00)00235-1, PMID: PubMed DOI

Hernandez B. S., Koh S.-C., Chial M., Focht D. D. (1997). Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8, 153–158. 10.1023/A:1008255218432 DOI

Huang A. C., Osbourn A. (2019). Plant terpenes that mediate below-ground interactions: prospects for bioengineering terpenoids for plant protection. Pest Manag. Sci. 75, 2368–2377. 10.1002/ps.5410, PMID: PubMed DOI PMC

Ishiguro T., Ohtake Y., Nakayama S., Inamori Y., Amagai T., Soma M., et al. . (2000). Biodegradation of dibenzofuran and dioxins by Pseudomonas aeruginosa and Xanthomonas maltophilia. Environ. Technol. 21, 1309–1316. 10.1080/09593330.2000.9619020 DOI

Kamanavalli C. M., Ninnekar H. Z. (2004). Biodegradation of DDT by a Pseudomonas species. Curr. Microbiol. 48, 10–13. 10.1007/s00284-003-4053-1, PMID: PubMed DOI

Kim S. Y., Jung J., Lim Y., Ahn J. H., Kim S. I., Hur H. G. (2003). Cis-2', 3'-dihydrodiol production on flavone B-ring by biphenyl dioxygenase from Pseudomonas pseudoalcaligenes KF707 expressed in Escherichia coli. Anton. Leeuw. Int. J. Gen. Mol. Microbiol. 84, 261–268. 10.1023/A:1026081824334, PMID: PubMed DOI

Kim J., Marshall M. R., Wei C.-I. (1995). Antibacterial activity of some essential oil components against five foodborne pathogens. J. Agric. Food Chem. 43, 2839–2845. 10.1021/jf00059a013 DOI

Kimura N., Kato H., Nishi A., Furukawa K. (1996). Analysis of substrate range of biphenyl-catabolic enzymes. Biosci. Biotechnol. Biochem. 60, 220–223. 10.1271/bbb.60.220, PMID: PubMed DOI

Koh C.-L., Sam C.-K., Yin W.-F., Tan L. Y., Krishnan T., Chong Y. M., et al. . (2013). Plant-derived natural products as sources of anti-quorum sensing compounds. Sensors 13, 6217–6228. 10.3390/s130506217, PMID: PubMed DOI PMC

Kumar P., Mohammadi M., Viger J. F., Barriault D., Gomez-Gil L., Eltis L. D., et al. . (2011). Structural insight into the expanded PCB-degrading abilities of a biphenyl dioxygenase obtained by directed evolution. J. Mol. Biol. 405, 531–547. 10.1016/j.jmb.2010.11.009, PMID: PubMed DOI PMC

Kweon O., Kim S.-J., Baek S., Chae J.-C., Adjei M. D., Baek D.-H., et al. . (2008). A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases. BMC Biochem. 9:11. 10.1186/1471-2091-9-11, PMID: PubMed DOI PMC

Leewis M.-C., Uhlik O., Fraraccio S., Mcfarlin K., Kottara A., Glover C., et al. . (2016). Differential impacts of willow and mineral fertilizer on bacterial communities and biodegradation in diesel fuel oil-contaminated soil. Front. Microbiol. 7:837. 10.3389/fmicb.2016.00837, PMID: PubMed DOI PMC

Lesic B., Rahme L. G. (2008). Use of the lambda red recombinase system to rapidly generate mutants in Pseudomonas aeruginosa. BMC Mol. Biol. 9:20. 10.1186/1471-2199-9-20, PMID: PubMed DOI PMC

Lin J. J., Smith M., Jessee J., Bloom F. (1992). DH11S: an Escherichia coli strain for preparation of single-stranded DNA from phagemid vectors. BioTechniques 12, 718–721. PMID: PubMed

Liu C.-W., Murray J. D. (2016). The role of flavonoids in nodulation host-range specificity: an update. Plants 5:33. 10.3390/plants5030033, PMID: PubMed DOI PMC

Marmulla R., Harder J. (2014). Microbial monoterpene transformations-a review. Front. Microbiol. 5:346. 10.3389/fmicb.2014.00346, PMID: PubMed DOI PMC

Martin V. J., Mohn W. W. (1999). A novel aromatic-ring-hydroxylating dioxygenase from the diterpenoid-degrading bacterium Pseudomonas abietaniphila BKME-9. J. Bacteriol. 181, 2675–2682. 10.1128/JB.181.9.2675-2682.1999, PMID: PubMed DOI PMC

Martinez J. L., Sánchez M. B., Martínez-Solano L., Hernandez A., Garmendia L., Fajardo A., et al. . (2009). Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol. Rev. 33, 430–449. 10.1111/j.1574-6976.2008.00157.x, PMID: PubMed DOI

Master E. R., Mohn W. W. (2001). Induction of bphA, encoding biphenyl dioxygenase, in two polychlorinated biphenyl-degrading bacteria, psychrotolerant Pseudomonas strain Cam-1 and mesophilic Burkholderia strain LB400. Appl. Environ. Microbiol. 67, 2669–2676. 10.1128/AEM.67.6.2669-2676.2001, PMID: PubMed DOI PMC

Mondello F. J., Turcich M. P., Lobos J. H., Erickson B. D. (1997). Identification and modification of biphenyl dioxygenase sequences that determine the specificity of polychlorinated biphenyl degradation. Appl. Environ. Microbiol. 63, 3096–3103. 10.1128/AEM.63.8.3096-3103.1997, PMID: PubMed DOI PMC

Mouz S., Merlin C., Springael D., Toussaint A. (1999). A GntR-like negative regulator of the biphenyl degradation genes of the transposon Tn4371. Mol. Gen. Genet. 262, 790–799. 10.1007/s004380051142, PMID: PubMed DOI

Musilova L., Ridl J., Polivkova M., Macek T., Uhlik O. (2016). Effects of secondary plant metabolites on microbial populations: changes in community structure and metabolic activity in contaminated environments. Int. J. Mol. Sci. 17:1205. 10.3390/ijms17081205, PMID: PubMed DOI PMC

Noma Y., Yamasaki S., Asakawa Y. (1992). Biotransformation of limonene and related compounds by Aspergillus cellulosae. Phytochemistry 31, 2725–2727. 10.1016/0031-9422(92)83619-A DOI

Ohtsubo Y., Delawary M., Takagi M., Ohta A., Kimbara K., Nagata Y. (2001). BphS, a key transcriptional regulator of bph genes involved in polychlorinated biphenyl/biphenyl degradation in Pseudomonas sp. KKS102. J. Biol. Chem. 276, 36146–36154. 10.1074/jbc.M100302200, PMID: PubMed DOI

Ohtsubo Y., Nagata Y., Kimbara K., Takagi M., Ohta A. (2000). Expression of the bph genes involved in biphenyl/PCB degradation in Pseudomonas sp. KKS102 induced by the biphenyl degradation intermediate, 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoic acid. Gene 256, 223–228. 10.1016/S0378-1119(00)00349-8, PMID: PubMed DOI

Palumbo J. D., Kado C. I., Phillips D. A. (1998). An isoflavonoid-inducible efflux pump in Agrobacterium tumefaciens is involved in competitive colonization of roots. J. Bacteriol. 180, 3107–3113. 10.1128/JB.180.12.3107-3113.1998, PMID: PubMed DOI PMC

Papadopoulos C. J., Carson C. F., Chang B. J., Riley T. V. (2008). Role of the MexAB-OprM efflux pump of Pseudomonas aeruginosa in tolerance to tea tree (Melaleuca alternifolia) oil and its monoterpene components terpinen-4-ol, 1,8-cineole, and alpha-terpineol. Appl. Environ. Microbiol. 74, 1932–1935. 10.1128/AEM.02334-07, PMID: PubMed DOI PMC

Parales R. E., Resnick S. M. (2006). “Aromatic Ring Hydroxylating Dioxygenases,” in Pseudomonas: Volume 4 Molecular Biology of Emerging Issues. eds. Ramos J.-L., Levesque R. C. (Boston, MA: Springer, US; ), 287–340.

Park Y.-I., So J., Koh S.-C. (1999). Induction by carvone of the polychlorinated biphenyl (PCB)-degradative pathway in Alcaligenes eutrophus H850 and its molecular monitoring. J. Microbiol. Biotechnol. 9, 804–810.

Parniske M., Ahlborn B., Werner D. (1991). Isoflavonoid-inducible resistance to the phytoalexin glyceollin in soybean rhizobia. J. Bacteriol. 173, 3432–3439. 10.1128/JB.173.11.3432-3439.1991, PMID: PubMed DOI PMC

Pham T. T. M., Pino Rodriguez N. J., Hijri M., Sylvestre M. (2015). Optimizing polychlorinated biphenyl degradation by flavonoid-induced cells of the rhizobacterium Rhodococcus erythropolis U23A. PLoS One 10:e0126033. 10.1371/journal.pone.0126033, PMID: PubMed DOI PMC

Pham T. T. M., Sylvestre M. (2013). Has the bacterial biphenyl catabolic pathway evolved primarily to degrade biphenyl? The diphenylmethane case. J. Bacteriol. 195:3563. 10.1128/JB.00161-13, PMID: PubMed DOI PMC

Pham T. T., Tu Y., Sylvestre M. (2012). Remarkable ability of Pandoraea pnomenusa B356 biphenyl dioxygenase to metabolize simple flavonoids. Appl. Environ. Microbiol. 78, 3560–3570. 10.1128/AEM.00225-12, PMID: PubMed DOI PMC

Prema B. R., Bhattacharyya P. K. (1962). Microbiological transformation of terpenes: II. transformation of alpha-pinene. Appl. Microbiol. 10, 524–528. PubMed PMC

Puentes-Cala E., Liebeke M., Markert S., Harder J. (2018). Limonene dehydrogenase hydroxylates the allylic methyl group of cyclic monoterpenes in the anaerobic terpene degradation by Castellaniella defragrans. J. Biol. Chem. 293, 9520–9529. 10.1074/jbc.RA117.001557, PMID: PubMed DOI PMC

Rausher M. D. (2001). Co-evolution and plant resistance to natural enemies. Nature 411, 857–864. 10.1038/35081193, PMID: PubMed DOI

Resnick S. M., Lee K., Gibson D. T. (1996). Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J. Ind. Microbiol. Biotechnol. 17, 438–457. 10.1007/BF01574775 DOI

Ridl J., Suman J., Fraraccio S., Hradilova M., Strejcek M., Cajthaml T., et al. . (2018). Complete genome sequence of Pseudomonas alcaliphila JAB1 (=DSM 26533), a versatile degrader of organic pollutants. Stand. Genomic Sci. 13:3. 10.1186/s40793-017-0306-7, PMID: PubMed DOI PMC

Robertson J. B., Spain J. C., Haddock J. D., Gibson D. T.C. (1992). Oxidation of nitrotoluenes by toluene dioxygenase: evidence for a monooxygenase reaction. Appli. Environ. Microbiol. 58, 2643–2648. 10.1128/AEM.58.8.2643-2648.1992 PubMed DOI PMC

Ryslava E., Krejcik Z., Macek T., Sykorova H., Denmerova K., Mackova M. (2003). Study of PCB degradation in real contaminated soil. Fresenius Environ. Bull. 12, 296–301.

Seo J., Kang S. I., Kim M., Han J., Hur H. G. (2011a). Flavonoids biotransformation by bacterial non-heme dioxygenases, biphenyl and naphthalene dioxygenase. Appl. Microbiol. Biotechnol. 91, 219–228. 10.1007/s00253-011-3334-z, PMID: PubMed DOI

Seo J., Kang S. I., Won D., Kim M., Ryu J. Y., Kang S. W., et al. . (2011b). Absolute configuration-dependent epoxide formation from isoflavan-4-ol stereoisomers by biphenyl dioxygenase of Pseudomonas pseudoalcaligenes strain KF707. Appl. Microbiol. Biotechnol. 89, 1773–1782. 10.1007/s00253-010-2989-1, PMID: PubMed DOI

Shaw L. J., Morris P., Hooker J. E. (2006). Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ. Microbiol. 8, 1867–1880. 10.1111/j.1462-2920.2006.01141.x, PMID: PubMed DOI

Singer A. C., Crowley D. E., Thompson I. P. (2003). Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol. 21, 123–130. 10.1016/S0167-7799(02)00041-0, PMID: PubMed DOI

Singer A. C., Gilbert E. S., Luepromchai E., Crowley D. E. (2000). Bioremediation of polychlorinated biphenyl-contaminated soil using carvone and surfactant-grown bacteria. Appl. Microbiol. Biotechnol. 54, 838–843. 10.1007/s002530000472, PMID: PubMed DOI

Speelmans G., Bijlsma A., Eggink G. (1998). Limonene bioconversion to high concentrations of a single and stable product, perillic acid, by a solvent-resistant Pseudomonas putida strain. Appl. Microbiol. Biotechnol. 50, 538–544. 10.1007/s002530051331 DOI

Taira K., Hirose J., Hayashida S., Furukawa K. (1992). Analysis of bph operon from the polychlorinated biphenyl-degrading strain of Pseudomonas pseudoalcaligenes KF707. J. Biol. Chem. 267, 4844–4853. 10.1016/S0021-9258(18)42908-0, PMID: PubMed DOI

Tandlich R., Brezná B., Dercová K. (2001). The effect of terpenes on the biodegradation of polychlorinated biphenyls by Pseudomonas stutzeri. Chemosphere 44, 1547–1555. 10.1016/S0045-6535(00)00523-3, PMID: PubMed DOI

Tellinghuisen J. (2001). Statistical error propagation. Chem. Eur. J. 105, 3917–3921. 10.1021/jp003484u DOI

Toussaint J. P., Pham T. T., Barriault D., Sylvestre M. (2012). Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. Appl. Microbiol. Biotechnol. 95, 1589–1603. 10.1007/s00253-011-3824-z, PMID: PubMed DOI

Triscari-Barberi T., Simone D., Calabrese F. M., Attimonelli M., Hahn K. R., Amoako K. K., et al. . (2012). Genome sequence of the polychlorinated-biphenyl degrader Pseudomonas pseudoalcaligenes KF707. J. Bacteriol. 194, 4426–4427. 10.1128/JB.00722-12, PMID: PubMed DOI PMC

Uhlik O., Wald J., Strejcek M., Musilova L., Ridl J., Hroudova M., et al. . (2012). Identification of bacteria utilizing biphenyl, benzoate, and naphthalene in long-term contaminated soil. PLoS One 7:e40653. 10.1371/journal.pone.0040653, PMID: PubMed DOI PMC

van Der Werf M. J., Orru R. V. A., Overkamp K. M., Swarts H. J., Osprian I., Steinreiber A., et al. . (1999). Substrate specificity and stereospecificity of limonene-1,2-epoxide hydrolase from Rhodococcus erythropolis DCL14; an enzyme showing sequential and enantioconvergent substrate conversion. Appl. Microbiol. Biotechnol. 52, 380–385. 10.1007/s002530051535 DOI

van Rensburg E., Moleleki N., Van Der Walt J. P., Botes P. J., Van Dyk M. S. (1997). Biotransformation of (+)limonene and (-)piperitone by yeasts and yeast-like fungi. Biotechnol. Lett. 19, 779–782. 10.1023/A:1018344411069 DOI

Vergani L., Mapelli F., Suman J., Cajthaml T., Uhlik O., Borin S. (2019). Novel PCB-degrading Rhodococcus strains able to promote plant growth for assisted rhizoremediation of historically polluted soils. PLoS One 14:e0221253. 10.1371/journal.pone.0221253, PMID: PubMed DOI PMC

Vezina J., Barriault D., Sylvestre M. (2008). Diversity of the C-terminal portion of the biphenyl dioxygenase large subunit. J. Mol. Microbiol. Biotechnol. 15, 139–151. 10.1159/000121326, PMID: PubMed DOI

Vuolo M. M., Lima V. S., Maróstica Junior M. R. (2019). “Chapter 2 - Phenolic Compounds: Structure, Classification, and Antioxidant Power,” in Bioactive Compounds. ed. Campos M. R. S. (Cambridge: Woodhead Publishing; ), 33–50.

Wald J., Hroudova M., Jansa J., Vrchotova B., Macek T., Uhlik O. (2015). Pseudomonads rule degradation of polyaromatic hydrocarbons in aerated sediment. Front. Microbiol. 6:1268. 10.3389/fmicb.2015.01268, PMID: PubMed DOI PMC

Watanabe T., Fujihara H., Furukawa K. (2003). Characterization of the second LysR-type regulator in the biphenyl-catabolic gene cluster of Pseudomonas pseudoalcaligenes KF707. J. Bacteriol. 185:7. 10.1128/JB.185.12.3575-3582.2003, PMID: PubMed DOI PMC

Watanabe T., Inoue R., Kimura N., Furukawa K. (2000). Versatile transcription of biphenyl catabolic bph operon in Pseudomonas pseudoalcaligenes KF707. J. Biol. Chem. 275, 31016–31023. 10.1074/jbc.M003023200, PMID: PubMed DOI

Xu H. X., Lee S. F. (2001). Activity of plant flavonoids against antibiotic-resistant bacteria. Phytother. Res. 15, 39–43. 10.1002/1099-1573(200102)15:1<39::AID-PTR684>3.0.CO;2-R, PMID: PubMed DOI

Differential effect of monoterpenes and flavonoids on the transcription of aromatic ring-hydroxylating dioxygenase genes in Rhodococcus opacus C1 and Rhodococcus sp. WAY2

Predominant Biphenyl Dioxygenase From Legacy Polychlorinated Biphenyl (PCB)-Contaminated Soil Is a Part of Unusual Gene Cluster and Transforms Flavone and Flavanone