Genomic and transcriptomic analyses of Agrobacterium tumefaciens S33 reveal the molecular mechanism of a novel hybrid nicotine-degrading pathway

Haiyan Huang,Huijun Xie,Huili Li,Shuning Wang,Rongshui Wang,Wenjun Yu

doi:10.1038/s41598-017-05320-1

Haiyan Huang, Huijun Xie + Show 4 more

Open Access

https://doi.org/10.1038/s41598-017-05320-1

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Abstract

Agrobacterium tumefaciens S33 is able to degrade nicotine via a novel hybrid of the pyridine and pyrrolidine pathways. It can be utilized to remove nicotine from tobacco wastes and transform nicotine into important functionalized pyridine precursors for some valuable drugs and insecticides. However, the molecular mechanism of the hybrid pathway is still not completely clear. Here we report the genome analysis of strain S33 and its transcriptomes grown in glucose-ammonium medium and nicotine medium. The complete gene cluster involved in nicotine catabolism was found to be located on a genomic island composed of genes functionally similar but not in sequences to those of the pyridine and pyrrolidine pathways, as well as genes encoding plasmid partitioning and replication initiation proteins, conjugal transfer proteins and transposases. This suggests that the evolution of this hybrid pathway is not a simple fusion of the genes involved in the two pathways, but the result of a complicated lateral gene transfer. In addition, other genes potentially involved in the hybrid pathway could include those responsible for substrate sensing and transport, transcription regulation and electron transfer during nicotine degradation. This study provides new insights into the molecular mechanism of the novel hybrid pathway for nicotine degradation.

Highlights

Microorganisms capable of degrading nicotine, a natural toxic alkaloid, have drawn much interest recently because they can be used to remove nicotine from tobacco industry wastes and tobacco products in an environmentally friendly fashion[1,2,3,4]
A number of nicotine-degrading bacteria have been isolated from different environments, the biochemical pathways and molecular mechanisms involved in nicotine catabolism were well characterized only in Arthrobacter sp. and Pseudomonas sp., which degrade nicotine through the pyridine pathway and the pyrrolidine pathway (Fig. 1a and c), respectively[1, 3, 11]
A. tumefaciens S33 degrades nicotine via a novel hybrid pathway of the traditional pyridine and pyrrolidine pathways

Summary

Introduction

Microorganisms capable of degrading nicotine, a natural toxic alkaloid, have drawn much interest recently because they can be used to remove nicotine from tobacco industry wastes and tobacco products in an environmentally friendly fashion[1,2,3,4]. A number of nicotine-degrading bacteria have been isolated from different environments, the biochemical pathways and molecular mechanisms involved in nicotine catabolism were well characterized only in Arthrobacter sp. Based on the identification of chemical intermediates and enzyme assays, we discovered that A. tumefaciens S33 discomposes nicotine via a novel fused nicotine degradation pathway, formed from the standard pyridine and pyrrolidine pathways (Fig. 1b)[2]. Oxidase (Hno) and 2,5-dihydroxypyridine dioxygenase (Hpo)] and sequencing genomes These studies have been integral in providing new information for a better understanding of the biochemical mechanism behind this novel hybrid nicotine degradation pathway, the molecular mechanism responsible for the pathway in these strains has not been completely elucidated. This study presents new results for elucidating the molecular mechanism of this novel hybrid nicotine degradation pathway

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