Unraveling metabolic flexibility of rhodococci in PCB transformation

• Published in: Chemosphere (Oxford) 2021-11, Vol.282, p.130975-130975, Article 130975
• Main Authors: Ines, Petrić, Vlasta, Drevenkar, Sanja, Fingler, Ana, Begonja Kolar, Dubravka, Hršak, Fabrice, Martin-Laurent, Nikolina, Udiković-Kolić
• Format: Article
• Language: English
• Subjects: Biotransformation; bph pathway; Life Sciences; Multiple pathways; Polychlorinated biphenyls; Rhodococcus; Transformation products
• ISSN: 0045-6535; 1879-1298
• DOI: 10.1016/j.chemosphere.2021.130975

Even though the genetic attributes suggest presence of multiple degradation pathways, most of rhodococci are known to transform PCBs only via regular biphenyl (bph) pathway. Using GC-MS analysis, we monitored products formed during transformation of 2,4,4′-trichlorobiphenyl (PCB-28), 2,2′,5,5′-tetrachlorobiphenyl (PCB-52) and 2,4,3′-trichlorobiphenyl (PCB-25) by previously characterized PCB-degrading rhodococci Z6, T6, R2, and Z57, with the aim to explore their metabolic pleiotropy in PCB transformations. A striking number of different transformation products (TPs) carrying a phenyl ring as a substituent, both those generated as a part of the bph pathway and an array of unexpected TPs, implied a curious transformation ability. We hypothesized that studied rhodococcal isolates, besides the regular one, use at least two alternative pathways for PCB transformation, including the pathway leading to acetophenone formation (via 3,4 (4,5) dioxygenase attack on the molecule), and a third sideway pathway that includes stepwise oxidative decarboxylation of the aliphatic side chain of the 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoate. Structure of the identified chlorinated benzoic acids and acetophenones allowed us to hypothesize that the first two pathways were the outcome of a ring-hydroxylating dioxygenase with the ability to attack both the 2,3 (5,6) and the 3,4 (4,5) positions of the biphenyl ring as well as dechlorination activity at both, -ortho and -para positions. We propose that several TPs produced by the bph pathway could have caused the triggering of the third sideway pathway. In conclusion, this study proposed ability of rhodococci to use different strategies in PCB transformation, which allows them to circumvent potential negative aspect of TPs on the overall transformation pathway. •Tested rhodococci use complex metabolic hub for PCB transformation.•Rhodococci use regular bph pathway in PCB transformation.•Alternative pathways works via production of acetophenones.•Third pathway includes stepwise oxidative decarboxylation of the aliphatic side chain of the HOPDA.•Rhodococci harbor specific ring-hydroxylating dioxygenase with dechlorination ability.