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Alternative Naphthalene Metabolic Pathway Includes Formation of ortho-Phthalic Acid and Cinnamic Acid Derivatives in the Rhodococcus opacus Strain 3D

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Abstract

Naphthalene, as a component of crude oil, is a common environmental pollutant. Biochemical and genetic aspects of naphthalene catabolism have been examined in most detail in the bacteria of Pseudomonas genus. In pseudomonads, the key intermediate in naphthalene degradation is salicylate. In this study, we investigated the ability of Rhodococcus opacus strain 3D to utilize naphthalene as a sole carbon and energy source. The characteristic feature of this strain is the inability to grow in the mineral medium supplemented with salicylate (typical intermediate of naphthalene degradation in Gram-negative bacteria). The absence of salicylate hydroxylase activity and salicylate accumulation in the course of R. opacus 3D cultivation in the mineral medium supplemented with naphthalene indicated existence of an alternative pathway of naphthalene oxidation. At the same time, R. opacus 3D was able to use monoaromatic compounds (salts of gentisic, ortho-phthalic, and 2-hydroxycinnamic acids and coumarin) as growth substrates. Based on the analysis of enzymatic activities, identification of the reaction intermediates, genetic determinants, and growth substrates, we concluded that R. opacus 3D carries out naphthalene degradation through an alternative pathway via formation of ortho-phthalic acid, which is untypical for pseudomonads. Using mass spectrometry, we showed for the first time that salicylic acid associate formed in trace amounts in the process of naphthalene degradation is not further metabolized and accumulated in the growth medium in a form of a dimer.

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Abbreviations

Cat 1,2-DO:

catechol 1,2- dioxygenase

Cat 2,3-DO:

catechol 2,3-dioxygenase

CFU:

colony-forming unit

GDO:

gentisate dioxygenase

MCI:

muconate cycloisomerase

NDO:

naphthalene 1,2-dioxygenase

PAH:

polycyclic aromatic hydrocarbon

PCA:

protocatechuic acid

PCA 3,4-DO:

pro-tocatechuate 3,4-dioxygenase

S1H:

salicylate 1-hydroxylase

TLC:

thin-layer chromatography

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Acknowledgements

The authors express their gratitude to Dr. M. I. Chernyavskaya (Belarusian State University, Minsk, Republic of Belarus) for kindly providing R. pyridinivorans 5Ap (L5A-BSU) strain and to Dr. E. G. Plotnikova (Institute of Ecology and Genetics of Microorganisms, Ural Division of the Russian Academy of Sciences, Perm, Russia) for kindly providing R. wratislaviensis G10 strain.

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  1. Pushchino Scientific Center for Biological Research, G. K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    T. O. Anokhina, T. Z. Esikova, A. B. Gafarov, V. N. Polivtseva, B. P. Baskunov & I. P. Solyanikova

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  1. T. O. Anokhina
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  2. T. Z. Esikova
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  3. A. B. Gafarov
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  6. I. P. Solyanikova
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Correspondence to I. P. Solyanikova.

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Russian Text © The Author(s), 2020, published in Biokhimiya, 2020, Vol. 85, No. 3, pp. 412–427.

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This work was supported by the Russian Foundation for Basic Research (project 18-34-00964).

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The authors declare no conflict of interest in financial or any other sphere.

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This article does not contain description of studies with human participants or animals performed by any of the authors.

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Anokhina, T.O., Esikova, T.Z., Gafarov, A.B. et al. Alternative Naphthalene Metabolic Pathway Includes Formation of ortho-Phthalic Acid and Cinnamic Acid Derivatives in the Rhodococcus opacus Strain 3D. Biochemistry Moscow 85, 355–368 (2020). https://doi.org/10.1134/S0006297920030116

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  • DOI: https://doi.org/10.1134/S0006297920030116

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