Biodegradation of Tetralin: Genomics, Gene Function and Regulation

Abstract

Tetralin (1,2,3,4-tetrahydonaphthalene) is a recalcitrant compound that consists of an aromatic and an alicyclic ring. It is found in crude oils, produced industrially from naphthalene or anthracene, and widely used as an organic solvent. Its toxicity is due to the alteration of biological membranes by its hydrophobic character and to the formation of toxic hydroperoxides. Two unrelated bacteria, Sphingopyxis granuli strain TFA and Rhodococcus sp. strain TFB were isolated from the same niche as able to grow on tetralin as the sole source of carbon and energy. In this review, we provide an overview of current knowledge on tetralin catabolism at biochemical, genetic and regulatory levels in both strains. Although they share the same biodegradation strategy and enzymatic activities, no evidences of horizontal gene transfer between both bacteria have been found. Moreover, the regulatory elements that control the expression of the gene clusters are completely different in each strain. A special consideration is given to the complex regulation discovered in TFA since three regulatory systems, one of them involving an unprecedented communication between the catabolic pathway and the regulatory elements, act together at transcriptional and posttranscriptional levels to optimize tetralin biodegradation gene expression to the environmental conditions.

Keywords: Rhodococcus sp. strain TFB; Sphingopyxis granuli strain TFA; carbon catabolite repression; redox proteins; tetralin.

Figure 1

Organization of the chromosomal thn genes in TFA. The arrows show the directions of gene transcription. Bent arrows represent the identified promoters. Dashed lines represent internal promoters.

Figure 2

Organization of the chromosomal thn genes in TFB. The arrows show the directions of gene transcription. Bent arrows represent the identified promoters.

Scheme 1

Tetralin catabolic pathway. Compound designations: 1, 1,2,3,4-tetrahydronaphthalene (Tetralin); 2, 1,2-dihydroxy-1,2,5,6,7,8-hexa-hydronaphthalene; 3, 1,2-dihydroxytetralin (DHT); 4, 4-(2-oxocyclohexyl)-2-hydroxybuta-2,4-dienoic acid (OCHBDA); 5, 2-hydroxydeca-2,4-dienedioic acid; 6, 2,4-dihydroxydec-2-ene-1,10-dioic acid (DHDDA); 7, 7-Oxoheptanoic acid (pimelic semialdehyde); 8, heptanedioic acid (pimelic acid); 9, pimeloyl-CoA; 10, 2,3-dehydropimeloyl-CoA; 11, 3-hydroxypimeloyl-CoA; 12, 3-oxopimeloyl-CoA; 13, glutaryl-CoA; 14, crotonyl-CoA. Proteins in brown correspond to those identified in TFB. Red lines show the cleavage of the rings.

Figure 3

Model for specific regulation and modulation of thn genes transcription in TFA. (a) In the presence of the tetralin, electrons are preferentially delivered to the dioxygenase and ThnY_ox and ThnR can activate transcription from the inducible thn promoters. (b) In the presence of compounds that are non-substrates of the dioxygenase, ThnA3 is accumulated in the reduced state and electrons are redirected towards ThnY instead of the dioxygenase impairing thn genes transcription.

Figure 4

Elements involved in carbon catabolite repression in TFA. High growth rate conditions like growth on a preferential carbon source like βHB and the presence of PHB granules have a positive effect on suhB transcription. This sRNA, together with Hfq, affects negatively ThnR translation in those conditions impeding induction of thn promoters (P_C, P_B, P_H and P_M) in the presence of tetralin. The presence of PHB granules themselves have a negative effect on thn induction. Doted and solid lines represent unknown and known mechanism, respectively.

Figure 5

Elements involved in carbon catabolite repression in TFB. In the absence of glucose and presence of tetralin, phosphorylated ThnS transfer the P group to ThnT which binds the ThnT box and induces thnA1 transcription. In the presence of glucose, a CRP-like protein binds CRP-like binding sites present at thnS and thnA1 promoters provoking a reduction in thnS transcription and impeding thnA1 transcriptional activation by phosphorylated ThnT.