Convergent evolution of the arginine deiminase pathway: the ArcD and ArcE arginine/ornithine exchangers.

Elke E E Noens,Juke S Lolkema

doi:10.1002/mbo3.412

Abstract

The arginine deiminase (ADI) pathway converts L‐arginine into L‐ornithine and yields 1 mol of ATP per mol of L‐arginine consumed. The L‐arginine/L‐ornithine exchanger in the pathway takes up L‐arginine and excretes L‐ornithine from the cytoplasm. Analysis of the genomes of 1281 bacterial species revealed the presence of 124 arc gene clusters encoding the pathway. About half of the clusters contained the gene encoding the well‐studied L‐arginine/L‐ornithine exchanger ArcD, while the other half contained a gene, termed here arcE, encoding a membrane protein that is not a homolog of ArcD. The arcE gene product of Streptococcus pneumoniae was shown to take up L‐arginine and L‐ornithine with affinities of 0.6 and 1 μmol/L, respectively, and to catalyze metabolic energy‐independent, electroneutral exchange. ArcE of S. pneumoniae could replace ArcD in the ADI pathway of Lactococcus lactis and provided the cells with a growth advantage. In contrast to ArcD, ArcE catalyzed translocation of the pathway intermediate L‐citrulline with high efficiency. A short version of the ADI pathway is proposed for L‐citrulline catabolism and the presence of the evolutionary unrelated arcD and arcE genes in different organisms is discussed in the context of the evolution of the ADI pathway.

Highlights

The arginine deiminase (ADI) pathway is the most widespread anaerobic route for arginine degradation (Zúňiga, Pérez, & González-Candelas, 2002)
The results show that uptake of L-arginine and L-ornithine by whole cells of L. lactis catalyzed by ArcD1 and ArcE is consistent with an electroneutral exchange process with a cytoplasmic substrate
ArcD and ArcE function as the L-arginine/L-ornithine exchangers in the pathway that take up the substrate L-arginine and excrete the product L-ornithine

Summary

| INTRODUCTION

The arginine deiminase (ADI) pathway is the most widespread anaerobic route for arginine degradation (Zúňiga, Pérez, & González-Candelas, 2002). L-arginine is converted into L-citrulline and ammonia, a reaction that is catalyzed by arginine deiminase (ADI, encoded by arcA). Since no metabolic energy is needed for the transport reaction, both substrates carry a single positive charge, ATP produced by the ADI pathway can be entirely used for other energy-demanding purposes. The four structural genes of the pathway are located in the center in the order arcA-arcB-arcD1-arcC1 in which arcD1 encodes the L-arginine/L-o rnithine exchanger. ArcD2 has been proposed to function as a putative L-arginine/L-a lanine exchanger in a partial L-arginine aminotransferase (ATA) pathway together with ArcT that was proposed to be an L-arginine-pyruvate transaminase

| EXPERIMENTAL PROCEDURES

Findings

| DISCUSSION