Recent Origin of the Methacrylate Redox System in Geobacter sulfurreducens AM-1 through Horizontal Gene Transfer.

Oksana V Arkhipova,Fyodor A Kondrashov,Marina V Zakharova,Margarita V Meer,Galina V Mikoulinskaia,Vasilii K Akimenko,Alexander S Galushko,Joel H Weiner

doi:10.1371/journal.pone.0125888

Abstract

The origin and evolution of novel biochemical functions remains one of the key questions in molecular evolution. We study recently emerged methacrylate reductase function that is thought to have emerged in the last century and reported in Geobacter sulfurreducens strain AM-1. We report the sequence and study the evolution of the operon coding for the flavin-containing methacrylate reductase (Mrd) and tetraheme cytochrome с (Mcc) in the genome of G. sulfurreducens AM-1. Different types of signal peptides in functionally interlinked proteins Mrd and Mcc suggest a possible complex mechanism of biogenesis for chromoproteids of the methacrylate redox system. The homologs of the Mrd and Mcc sequence found in δ-Proteobacteria and Deferribacteres are also organized into an operon and their phylogenetic distribution suggested that these two genes tend to be horizontally transferred together. Specifically, the mrd and mcc genes from G. sulfurreducens AM-1 are not monophyletic with any of the homologs found in other Geobacter genomes. The acquisition of methacrylate reductase function by G. sulfurreducens AM-1 appears linked to a horizontal gene transfer event. However, the new function of the products of mrd and mcc may have evolved either prior or subsequent to their acquisition by G. sulfurreducens AM-1.

Highlights

Anaerobic bacteria frequently use unsaturated organic compounds as terminal electron acceptors [1]
The G. sulfurreducens AM-1 strain is capable of complete oxidation of acetate coupled to reduction of methacrylate (2-methylpropenoate), an anthropogenic compound that serves as the terminal acceptor of the bacterial reductase chain [18]
We sequenced the genome of G. sulfurreducens AM-1, obtaining a draft with a single contig

Summary

Introduction

Anaerobic bacteria frequently use unsaturated organic compounds as terminal electron acceptors [1]. The G. sulfurreducens AM-1 strain is capable of complete oxidation of acetate coupled to reduction of methacrylate (2-methylpropenoate), an anthropogenic compound that serves as the terminal acceptor of the bacterial reductase chain [18]. The study of Geobacter species (Deltaproteobacteria) is of applied interest due to their significant role in bioremediation of radioactive metals [19,20,21,22] They serve as important agents in the global cycles of metals and carbon, reducing Fe(III) to Fe(II) and U(VI) to U(IV), oxidizing acetate and other organic compounds and participating in humus decomposition. They are fumarate-respiring organisms [19,20,21,23] and electrotrophs [24]. We report the sequence of the two genes of the methacrylate redox system from the G. sulfurreducens АМ-1 genome, analyze their translation products and study their evolutionary origins

Results

Discussion

Experimental Procedures