Ecological Roles of Arc Signal Transduction System Revealed by Evolutionary Genetics Analysis

Research Article

J Bacteriol Mycol. 2014;1(2): 8.

Ecological Roles of Arc Signal Transduction System Revealed by Evolutionary Genetics Analysis

Yangyang Dong, Fen Wan, Jianhua Yin and Haichun Gao*

Institute of Microbiology and College of Life Sciences, Zhejiang University, China

*Corresponding author: Haichun Gao, Institute of Microbiology and College of Life Sciences, Zhejiang University, China

Zhang H, Z-BioMed, Inc., 15725 Crabbs Branch Way, Rockville, MD 20855, USA.

Received: August 14, 2014; Accepted: November 06, 2014; Published: November 12, 2014


The Arc signal transduction system was studied in γ-proteobacteria to determine evolutionary mechanisms and ecological pressures responsible for the plasticity of this system. Phylogenic analysis of the arcA gene encoding the DNA-binding response regulator suggests that the gene has remained under strong purifying selection throughout its history while the arcB gene encoding the sensor histidine kinase has undergone extensive modification in various lineages. The major observed modification occurs in the Alteromonadaceae family, where the Hpt domain of ArcB has been uncoupled from the sensor component in several genera (Shewanella, Colwellia and Idiomarina). This phenomenon appears to be linked to the free-living lifestyles of the Alteromonads. In contrast to the prevailing view of the Arc system existing only in facultative anaerobes, several of the Alteromonad species which encode Arc systems are strict aerobes or aero-tolerant anaerobes, suggesting additional functions for the Arc system beyond facultative anaerobiosis. Molecular clock estimates using linearized phylogenetics trees for the arcA gene place the origins of the system at 600-1300 million years ago, a period roughly corresponding to the rise in atmospheric oxygen levels that occurred in the Precambrian Era. It is hypothesized that the Arc system originated as an early oxidative stress response mechanism in the γ-proteobacteria and was later co-opted for the facultative anaerobic lifestyle.

Keywords: Shewanella; Alteromonaceae; Arc System; Signal Transduction; Molecular


The metabolic transition to anaerobiosis in γ-proteobacterial species, such as model microorganism Escherichia coli, is mediated in part by the aerobic respiratory control (Arc) phosphorelay twocomponent system (TCS) consisting of a hybrid sensor histidine kinase (ArcB) and a global OmpR-family winged-helix response regulator (ArcA) [1, 2] (Figure 1). Reduction of the quinone pool in response to anaerobiosis triggers auto-phosphorylation of ArcB, which initiates a phosphorelay from the histidine kinase dimerization (HisKA) domain (ArcB, H292) to the receiver domain (ArcB, D576) to the Hpt domain (ArcB, H717) and finally to the ArcA receiver domain (D54) [3,4]. Most ArcB proteins also contain a PAS domain of unknown function, though this domain has lost in the Pasteurellaceae [5]. ArcA serves primarily as a global repressor of aerobic metabolic pathways, but recent studies have shown that the ArcA regulon is significantly more varied than was previously believed [6-15].

A major exception to the canonical γ-proteobacterial Arc system was observed in Shewanella oneidensis [9]. Shewanella species are facultative anaerobes of the Altermonadaceae family that utilize numerous compounds for respiration, including nitrate, DMSO, insoluble iron oxides and a variety of heavy metal ions [16]. An analysis of the genomic sequence of S. oneidensis revealed a gene encoding a putative ArcA homolog with 81% amino acid sequence identity to the E. coli ArcA protein. Despite the presence of an experimentally verified ArcA, annotation of the genome has not revealed a full-length arcB gene. Instead, signal transduction to ArcA is initiated by ArcS, which displays substantial sequence and structure variation fromE. coli ArcB [17, 18] (Figure 1). The most striking difference betweenE. coli ArcB and ArcS with respect to phosphorelay is that the latter lacks the Hpt domain. To compensate for the loss, S. oneidensis employs a free HptA protein with homology to the Hpt domain of E. coli ArcB [9]. Consistent with this, the ArcA regulon of S. oneidensis is substantially different from that of E. coli although their DNA-binding motifs are similar [11, 19]. Therefore, the cumulative computational and experimental results show that the Arc system of Shewanella has undergone significant evolution since the divergence of the lineage from the Enterobacteria.