A soil bacterial catabolic pathway on the move: Transfer of nicotine catabolic genes between Arthrobacter genus megaplasmids and invasion by mobile elements

The 165,137 bp plasmid pAO1 of Paenarthrobacter nicotinovorans carries the genes of a nicotine catabolic pathway. The genes are organized into several gene modules responsible for the catabolism of l - and d -nicotine to nicotine blue, α-ketoglutarate and succinate. Various modules of these genes have been shown to be present in gram-positive (Gram+) soil bacteria. The presence of the identical pAO1 nic -genes on the 288,370 bp plasmid pZXY21 of Arthrobacter sp. ZXY2 (96% to 100% at the nucleotide level) permitted the identification of the limits of this DNA fragment. At the 5′ end of the nic -genes are located the ORFs of two predicted integrases of the tyrosine recombinase family with conserved R, H, R and Y catalytic residues and that of a small transposase with a predicted leucine zipper motive. They are related to Tn 554 A, Tn 554 B and Tn 554 C of Staphylococcus aureus and suggest that the entire nic -genes DNA fragment represents a large catabolic transposon. Surprisingly the nic -genes on pZXY21 were found to be interspersed by mobile elements encoding transposases of various IS families. Insertion of these IS elements disrupts nicotine degradation and divide the nic -genes DNA into potentially new transposons. This finding may illustrate how nicotine catabolic genes can be mobilized and spread by horizontal gene transfer to other soil bacteria.