Microbial Degradation of Pyridine: a Complete Pathway inArthrobactersp. Strain 68b Deciphered

Abstract

Pyridine and its derivatives constitute the majority of heterocyclic aromatic compounds that occur largely as a result of human activities and contribute to environmental pollution. It is known that they can be degraded by various bacteria in the environment; however, the degradation of unsubstituted pyridine has not yet been completely resolved. In this study, we present data on the pyridine catabolic pathway in Arthrobacter sp. strain 68b at the level of genes, enzymes, and metabolites. The pyr gene cluster, responsible for the degradation of pyridine, was identified in a catabolic plasmid, p2MP. The pathway of pyridine metabolism consisted of four enzymatic steps and ended by the formation of succinic acid. The first step in the degradation of pyridine proceeds through a direct ring cleavage catalyzed by a two-component flavin-dependent monooxygenase system, encoded by pyrA (pyridine monooxygenase) and pyrE genes. The genes pyrB, pyrC, and pyrD were found to encode (Z)-N-(4-oxobut-1-enyl)formamide dehydrogenase, amidohydrolase, and succinate semialdehyde dehydrogenase, respectively. These enzymes participate in the subsequent steps of pyridine degradation. The metabolites of these enzymatic reactions were identified, and this allowed us to reconstruct the entire pyridine catabolism pathway in Arthrobacter sp. 68b. IMPORTANCE The biodegradation pathway of pyridine, a notorious toxicant, is relatively unexplored, as no genetic data related to this process have ever been presented. In this paper, we describe the plasmid-borne pyr gene cluster, which includes the complete set of genes responsible for the degradation of pyridine. A key enzyme, the monooxygenase PyrA, which is responsible for the first step of the catabolic pathway, performs an oxidative cleavage of the pyridine ring without typical activation steps such as reduction or hydroxylation of the heterocycle. This work provides new insights into the metabolism of N-heterocyclic compounds in nature.

Integrated Metabolomic and Transcriptomic Analysis of Acute Kidney Injury Caused by Leptospira Infection

“…and Arthrobacter sp. Strain 68b [ 24 , 25 ]. Importantly, a putative nicotine degradation pathway was identified in pathogenic L. interrogans .…”

A novel soluble di‐iron monooxygenase from the soil bacterium Solimonas soli

“…Monooxygenases (MOs) initiate the metabolism of hydrocarbons in many bacteria and play critical roles in biogeochemistry via the oxidation of methane and ammonia in the carbon and nitrogen cycles, respectively (Ayub et al, 2022; Greening & Grinter, 2022; Lu et al, 2020). MOs can biodegrade diverse pollutants and xenobiotics, including aliphatic (Abbasian et al, 2015) and aromatic (Seo et al, 2009) hydrocarbons, haloalkenes (Le & Coleman, 2011), haloalkanes (Hage & Hartmans, 1999), cyclic ethers (Masuda et al, 2012a) and other heterocyclic compounds (Casaite et al, 2020; Thiemer et al, 2003). The MO enzymes are valuable for biocatalysis due to their ability to insert oxygen atoms into inert substrates with high regioselectivity and enantioselectivity (Birolli et al, 2019; Cheung et al, 2013; Desai et al, 2016; Koeller & Wong, 2001; Leak et al, 2009; Torres Pazmino et al, 2010).…”

Expression and Characterization of 3,6-Dihydroxy-picolinic Acid Decarboxylase PicC of Bordetella bronchiseptica RB50

“…These pyridine derivatives compounds are widely distributed in soil, water, and sediment. Microorganisms could decompose and use them as sole carbon or nitrogen sources, and in the meantime, reduce the concentrations of those toxic compounds [1][2][3][4][5].…”

“…The PA degradation pathway and pic gene cluster responsible for PA catabolism have been studied in Gram-negative strain Alcaligenes faecalis JQ135 (Figure 1) [12,13]. The upper pathway contains intermediates 6-hydroxypicolinic acid (6HPA) and 3,6-dihydroxypicolinic acid (3,6DHPA), which are catalyzed by PA dehydrogenase (PicA) and 6HPA monooxygenase (PicB). The lower pathway was 2,5-dihydroxypyridine (2,5DHP) to fumaric acid (a Krebs cycle intermediate), which was catalyzes by four conserved enzymes, 2,5DHP 5,6-dioxygenase (PicD), N-formylmaleamic acid deformylase (PicE), maleamic acid amidohydrolase (PicF), and maleic acid isomerase (PicG).…”