Abstract
Biodegradation of an anthropogenic herbicide, 2,4-dichlorophenoxyacetic acid (2,4-D), was documented in the 1950s, the early age of its usage. The 2,4-D-degradative genes in bacteria have long been studied since the first report was published in the 1980s. The well-known 2,4-D catabolic gene cluster tfdABCDFE on the plasmid pJP4 was originally isolated from Cupriavidus pinatubonensis JMP134 and is found to be widely distributed among the phylum Proteobacteria. 2,4-D catabolic gene cluster in pJP4 possesses some distinguished features for the effective degradation and dissemination, e.g., complete gene set located on one site, duplication of the toxic chlorophenol degradation pathway genes, and its self-transmissibility. The dioxygenase gene, tfdA, that catalyzes the initial step of 2,4-D degradation is a distinctive gene in this system on the point that neither similar nucleotide sequence gene nor similar function enzyme was discovered in the environment. tfdA has been used as a good marker or reporter gene for identifying or detecting the 2,4-D degradation system. However, two decades later, a novel 2,4-D degradation gene system, cad gene cluster, was identified from Bradyrhizobium sp. strain HW13 in the 2000s. This finding and subsequent studies changed our whole view of 2,4-D metabolism as tfd gene cluster had long been believed to be an exclusive system responsible for 2,4-D degradation. The initial dioxygenase gene cadA is completely different from tfdA and is a member of aromatic ring hydroxylation dioxygenase genes. In contrast to tfd gene carriers, it is notable that the first organism carrying cadA was discovered from non-2,4-D-contaminated pristine environment. To date, cad system is known to be widespread in the genera Bradyrhizobium and Sphingomonas and perhaps more diverse organisms. In this chapter, we overview the fundamental features, distribution, and competitiveness of those two representative 2,4-D gene systems based upon genetic and biochemical studies together with culture-independent molecular community analyses.
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References
Bælum J, Jacobsen CS, Holben WE (2010) Comparison of 16S rRNA gene phylogeny and functional tfdA gene distribution in thirty-one different 2,4-dichlorophenoxyacetic acid and 4-chloro-2-methylphenoxyacetic acid degraders. Syst Appl Microbiol 33(2):67–70. doi:10.1016/j.syapm. 2010.01.001
Bathe S, Lebuhn M, Ellwart JW, Wuertz S, Hausner M (2004) High phylogenetic diversity of transconjugants carrying plasmid pJP4 in an activated sludge-derived microbial community. FEMS Microbiol Lett 235(2):215–219. doi:10.1016/j.femsle.2004.04.038
Bhat MA, Tsuda M, Horiike K, Nozaki M, Vaidyanathan CS, Nakazawa T (1994) Identification and characterization of a new plasmid carrying genes for degradation of 2,4-dichlorophenoxyacetate from Pseudomonas cepacia CSV90. Appl Environ Microbiol 60(1):307–312
Cupples AM, Sims GK (2007) Identification of in situ 2,4-dichlorophenoxyacetic acid-degrading soil microorganisms using DNA-stable isotope probing. Soil Biol Biochem 39(1):232–238. doi:10.1016/j.soilbio.2006.07.011
Danganan CE, Shankar S, Ye RW, Chakrabarty AM (1995) Substrate diversity and expression of the 2,4,5-trichlorophenoxyacetic acid oxygenase from Burkholderia cepacia AC1100. Appl Environ Microbiol 61(12):4500–4504
DiGiovanni GD, Neilson JW, Pepper IL, Sinclair NA (1996) Gene transfer of Alcaligenes eutrophus JMP134 plasmid pJP4 to indigenous soil recipients. Appl Environ Microbiol 62(7):2521–2526
Don RH, Pemberton JM (1981) Properties of six pesticide degradation plasmids isolated from Alcaligenes paradoxus and Alcaligenes eutrophus. J Bacteriol 145(2):681–686
Don RH, Pemberton JM (1985) Genetic and physical map of the 2,4-dichlorophenoxyacetic acid-degradative plasmid pJP4. J Bacteriol 161(1):466–468
Don RH, Weightman AJ, Knackmuss HJ, Timmis KN (1985) Transposon mutagenesis and cloning analysis of the pathways for degradation of 2,4-dichlorophenoxyacetic acid and 3-chlorobenzoate in Alcaligenes eutrophus JMP134(pJP4). J Bacteriol 161(1):85–90
Dunbar J, White S, Forney L (1997) Genetic diversity through the looking glass: effect of enrichment bias. Appl Environ Microbiol 63(4):1326–1331
Duxbury JM, Tiedje JM, Alexande M, Dawson JE (1970) 2,4-D metabolism: enzymatic conversion of chloromaleylacetic acid to succinic acid. J Agric Food Chem 18(2):199. doi:10.1021/jf60168a029
Filer K, Harker AR (1997) Identification of the inducing agent of the 2,4-dichlorophenoxyacetic acid pathway encoded by plasmid pJP4. Appl Environ Microbiol 63(1):317–320
Fulthorpe RR, McGowan C, Maltseva OV, Holben WE, Tiedje JM (1995) 2,4-Dichlorophenoxyacetic acid-degrading bacteria contain mosaics of catabolic genes. Appl Environ Microbiol 61(9):3274–3281
Fulthorpe RR, Rhodes AN, Tiedje JM (1996) Pristine soils mineralize 3-chlorobenzoate and 2,4-dichlorophenoxyacetate via different microbial populations. Appl Environ Microbiol 62(4):1159–1166
Harker AR, Olsen RH, Seidler RJ (1989) Phenoxyacetic acid degradation by the 2,4-dichlorophenoxyacetic acid (TFD) pathway of plasmid pJP4: mapping and characterization of the TFD regulatory gene, tfdR. J Bacteriol 171(1):314–320
Hoffmann D, Kleinsteuber S, Muller RH, Babel W (2003) A transposon encoding the complete 2,4-dichlorophenoxyacetic acid degradation pathway in the alkalitolerant strain Delftia acidovorans P4a. Microbiology 149:2545–2556. doi:10.1099/mic.0.026260-0
Hogan DA, Buckley DH, Nakatsu CH, Schmidt TM, Hausinger RP (1997) Distribution of the tfdA gene in soil bacteria that do not degrade 2,4-dichlorophenoxyacetic acid (2,4-D). Microb Ecol 34(2):90–96. doi:10.1007/s00248998
Hotopp JCD, Hausinger RP (2001) Alternative substrates of 2.4-dichlorophenoxyacetate/alpha-ketoglumate dioxygenase. J Mol Catal B: Enzym 15(4–6):155–162
Inoue T, Sakakibara F, Handa M, Suzuki T, Takeda M, Hayashi A, Murakoshi Z (1988) Herbicides. In: Inoue T (ed) Nouyaku-gaku. Hirokawa Publishing Co., Tokyo
Itoh K, Kanda R, Sumita Y, Kim H, Kamagata Y, Suyama K, Yamamoto H, Hausinger RP, Tiedje JM (2002) tfdA-like genes in 2,4-dichlorophenoxyacetic acid-degrading bacteria belonging to the Bradyrhizobium-Agromonas-Nitrobacter-Afipia cluster in alpha-proteobacteria. Appl Environ Microbiol 68(7):3449–3454. doi:10.1128/aem.68.7.3449-3454.2002
Itoh K, Tashiro Y, Uobe K, Kamagata Y, Suyama K, Yamamoto H (2004) Root nodule Bradyrhizobium spp. Harbor tfdA alpha and cadA, homologous with genes encoding 2,4-dichlorophenoxyacetic acid-degrading proteins. Appl Environ Microbiol 70(4):2110–2118. doi:10.1128/a-em.70.4.2110-2118.2004
Ka JO, Holben WE, Tiedje JM (1994) Genetic and phenotypic diversity of 2,4-dichlorophenoxyacetic acid (2,4-D)-degrading bacteria isolated from 2,4-D-treated field soils. Appl Environ Microbiol 60(4):1106–1115
Kamagata Y, Fulthorpe RR, Tamura K, Takami H, Forney LJ, Tiedje JM (1997) Pristine environments harbor a new group of oligotrophic 2,4-dichlorophenoxyacetic acid-degrading bacteria. Appl Environ Microbiol 63(6):2266–2272
Kaphammer B, Kukor JJ, Olsen RH (1990) Regulation of tfdCDEF by tfdR of the 2,4-dichlorophenoxyacetic acid degradation plasmid pJP4. J Bacteriol 172(5):2280–2286
Kitagawa W, Takami S, Miyauchi K, Masai E, Kamagata Y, Tiedje JM, Fukuda M (2002) Novel 2,4-dichlorophenoxyacetic acid degradation genes from oligotrophic Bradyrhizobium sp. strain HW13 isolated from a pristine environment. J Bacteriol 184(2):509–518. doi:10.1128/jb.184.2.509-518.2002
Laemmli CM, Leveau JHJ, Zehnder AJB, van der Meer JR (2000) Characterization of a second tfd gene cluster for chlorophenol and chlorocatechol metabolism on plasmid pJP4 in Ralstonia eutropha JMP134(pJP4). J Bacteriol 182(15):4165–4172. doi:10.1128/jb.182.15.4165-4172.2000
Ledger T, Pieper DH, Gonzalez B (2006) Chlorophenol hydroxylases encoded by plasmid pJP4 differentially contribute to chlorophenoxy acetic acid degradation. Appl Environ Microbiol 72(4):2783–2792. doi:10.1128/aem.72.4.2783-2792.2006
Lee TH, Kurata S, Nakatsu CH, Kamagata Y (2005) Molecular analysis of bacterial community based on 16S rDNA and functional genes in activated sludge enriched with 2,4-dichlorophenoxyacetic acid (2,4-d) under different cultural conditions. Microb Ecol 49(1):151–162. doi:10.1007/s00248-003-1035-6
Leveau JHJ, van der Meer JR (1996) The tfdR gene product can successfully take over the role of the insertion element-inactivated TfdT protein as a transcriptional activator of the tfdCDEF gene cluster, which encodes chlorocatechol degradation in Ralstonia eutropha JMP134(pJP4). J Bacteriol 178(23):6824–6832
Leveau JHJ, van der Meer JR (1997) Genetic characterization of insertion sequence ISJP4 on plasmid pJP4 from Ralstonia eutropha JMP134. Gene 202(1–2):103–114. doi:10.1016/s0378-1119(97)00460-5
Leveau JHJ, Zehnder AJB, van der Meer JR (1998) The tfdK gene product facilitates uptake of 2,4-dichlorophenoxyacetate by Ralstonia eutropha JMP134(pJP4). J Bacteriol 180(8):2237–2243
Leveau JHJ, Konig F, Fuchslin H, Werlen C, van der Meer JR (1999) Dynamics of multigene expression during catabolic adaptation of Ralstonia eutropha JMP134 (pJP4) to the herbicide 2,4-dichlorophenoxyacetate. Mol Microbiol 33(2):396–406. doi:10.1046/j.1365-2958.1999.01483.x
Lykidis A, Pérez-Pantoja D, Ledger T, Mavromatis K, Anderson IJ, Ivanova NN, Hooper SD, Lapidus A, Lucas S, González B, Kyrpides NC (2010) The complete multipartite genome sequence of Cupriavidus necator JMP134, a versatile pollutant degrader. PLoS One 5(3):e9729
Mae AA, Marits RO, Ausmees NR, Koiv VM, Heinaru AL (1993) Characterization of a new 2,4-dichlorophenoxyacetic acid degrading plasmid pEST4011: physical map and localization of catabolic genes. J Gen Microbiol 139:3165–3170
McGowan C, Fulthorpe R, Wright A, Tiedje JM (1998) Evidence for interspecies gene transfer in the evolution of 2,4-dichlorophenoxyacetic acid degraders. Appl Environ Microbiol 64(10):4089–4092
Neilson JW, Josephson KL, Pepper IL, Arnold RB, Digiovanni GD, Sinclair NA (1994) Frequency of horizontal gene transfer of a large catabolic plasmid (pJP4) in soil. Appl Environ Microbiol 60(11):4053–4058
Newby DT, Josephson KL, Pepper IL (2000) Detection and characterization of plasmid pJP4 transfer to indigenous soil bacteria. Appl Environ Microbiol 66(1):290–296
Pérez-Pantoja D, Guzmán L, Manzano M, Pieper DH, González B (2000) Role of tfdC I D I E I F I and tfdD II C II E II F II gene modules in catabolism of 3-chlorobenzoate by Ralstonia eutropha JMP134(pJP4). Appl Environ Microbiol 66(4):1602–1608. doi:10.1128/aem.66.4.1602-1608.2000
Poh RPC, Smith ARW, Bruce IJ (2002) Complete characterisation of Tn5530 from Burkholderia cepacia strain 2a (pIJB1) and studies of 2,4-dichlorophenoxyacetate uptake by the organism. Plasmid 48(1):1–12. doi:10.1016/s0147-619x(02)00018-5
Sen D, Yano H, Suzuki H, Król JE, Rogers L, Brown CJ, Top EM (2010) Comparative genomics of pAKD4, the prototype IncP-1δ plasmid with a complete backbone. Plasmid 63(2):98–107
Shimojo M, Kawakami M, Amada K (2009) Analysis of genes encoding the 2,4-dichlorophenoxyacetic acid-degrading enzyme from Sphingomonas agrestis 58–1. J Biosci Bioeng 108(1):56–59. doi:10.1016/j.jbiosc.2009.02.018
Steenson TI, Walker N (1957) The pathway of breakdown of 2:4-dichloro- and 4-chloro-2-methyl-phenoxyacetic acid by bacteria. J Gen Microbiol 16(1):146–155. doi:10.1099/00221287-16-1-146
Suwa Y, Wright AD, Fukimori F, Nummy KA, Hausinger RP, Holben WE, Forney LJ (1996) Characterization of a chromosomally encoded 2,4-dichlorophenoxyacetic acid alpha-ketoglutafate dioxygenase from Burkholderia sp strain RASC. Appl Environ Microbiol 62(7):2464–2469
Trefault N, Clement P, Manzano M, Pieper DH, González B (2002) The copy number of the catabolic plasmid pJP4 affects growth of Ralstonia eutropha JMP134 (pJP4) on 3-chlorobenzoate. FEMS Microbiol Lett 212(1):95–100. doi:Pii s0378-1097(02)00734-6 10.1016/s0378-1097(02)00734-6
Trefault N, De la Iglesia R, Molina AM, Manzano M, Ledger T, Pérez-Pantoja D, Sánchez MA, Stuardo M, González B (2004) Genetic organization of the catabolic plasmid pJP4 from Ralstonia eutropha JMP134 (pJP4) reveals mechanisms of adaptation to chloroaromatic pollutants and evolution of specialized chloroaromatic degradation pathways. Environ Microbiol 6(7):655–668. doi:10.1111/j.1462-2920.2004.00596.x
Trefault N, Guzman L, Perez H, Godoy M, Gonzalez B (2009) Involvement of several transcriptional regulators in the differential expression of tfd genes in Cupriavidus necator JMP134. Int Microbiol 12(2):97–106. doi:10.2436/20.1501.01.86
Vallaeys T, Courde L, Mc Gowan C, Wright AD, Fulthorpe RR (1999) Phylogenetic analyses indicate independent recruitment of diverse gene cassettes during assemblage of the 2,4-D catabolic pathway. FEMS Microbiol Ecol 28(4):373–382. doi:10.1111/j.1574-6941.1999.tb00591.x
Vedler E, Vahter M, Heinaru A (2004) The completely sequenced plasmid pEST4011 contains a novel IncP1 backbone and a catabolic transposon harboring tfd genes for 2,4-dichlorophenoxyacetic acid degradation. J Bacteriol 186(21):7161–7174. doi:10.1128/jb.186.21.7161-7174.2004
You IS, Ghosal D (1995) Genetic and molecular analysis of a regulatory region of the herbicide 2,4-dichlorophenoxyacetate catabolic plasmid pJP4. Mol Microbiol 16(2):321–331. doi:10.1111/j.1365-2958.1995.tb02304.x
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Kitagawa, W., Kamagata, Y. (2014). Diversity of 2,4-Dichlorophenoxyacetic Acid (2,4-D)-Degradative Genes and Degrading Bacteria. In: Nojiri, H., Tsuda, M., Fukuda, M., Kamagata, Y. (eds) Biodegradative Bacteria. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54520-0_3
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