The Mercury Resistance Operon: From an Origin in a Geothermal Environment to an Efficient Detoxification Machine

Abstract

Mercuric mercury (Hg[II]) is a highly toxic and mobile element that is likely to have had a pronounced and adverse effect on biology since Earth’s oxygenation ∼2.4 billion years ago due to its high affinity for protein sulfhydryl groups, which upon binding destabilize protein structure and decrease enzyme activity, resulting in a decreased organismal fitness. The central enzyme in the microbial mercury detoxification system is the mercuric reductase (MerA) protein, which catalyzes the reduction of Hg(II) to volatile Hg(0). In addition to MerA, mer operons encode for proteins involved in regulation, Hg binding, and organomercury degradation. Mer-mediated approaches have had broad applications in the bioremediation of mercury-contaminated environments and industrial waste streams. Here, we examine the composition of 272 individual mer operons and quantitatively map the distribution of mer-encoded functions on both taxonomic SSU rRNA gene and MerA phylogenies. The results indicate an origin and early evolution of MerA among thermophilic bacteria and an overall increase in the complexity of mer operons through evolutionary time, suggesting continual gene recruitment and evolution leading to an improved efficiency and functional potential of the Mer detoxification system. Consistent with a positive relationship between the evolutionary history and topology of MerA and SSU rRNA gene phylogenies (Mantel R = 0.81, p < 0.01), the distribution of the majority of mer functions, when mapped on these phylograms, indicates an overall tendency to inherit mer-encoded functions through vertical descent. However, individual mer functions display evidence of a variable degree of vertical inheritance, with several genes exhibiting strong evidence for acquisition via lateral gene transfer and/or gene loss. Collectively, these data suggest that (i) mer has evolved from a simple system in geothermal environments to a widely distributed and more complex and efficient detoxification system, and (ii) merA is a suitable biomarker for examining the functional diversity of Hg detoxification and for predicting the composition of mer operons in natural environments.

A Novel Mercuric Reductase from the Unique Deep Brine Environment of Atlantis II in the Red Sea

“…Despite the availability of detailed information concerning the structure-function relationships of MerA, and compelling phylogenetic evidence indicating that MerA originated and evolved in thermophilic microorganisms residing in geothermal environments (15,16), to our knowledge, no thermophilic and/or halophilic MerA homolog derived from such an environment has yet been characterized in detail.…”

Diversity of Mercury Resistant Escherichia coli Strains Isolated from Aquatic Systems in Rio de Janeiro, Brazil

“…Variability within merA gene has been described, and diverse MerA protein homologs have been identified in both archaeal as well as bacterial genomes but not in eukaryal genomes [17]. The increased complexity of mer operons can be attributed to the gradual addition of functions involved in the regulation of the operon by Hg, Hg transport, and organomercury resistance [17]. The diversity of merA gene in Gram-negative and Gram-positive bacteria has been accessed by several approaches including those using restriction fragment assays [27,31,33,34].…”

“…DGGE fingerprinting is a technique widely used in microbial ecology studies and has been focused on studies of genetic diversity and bacterial communities from several environments [17,42]. Variability within merA gene has been described, and diverse MerA protein homologs have been identified in both archaeal as well as bacterial genomes but not in eukaryal genomes [17].…”

“…In presence of Hg 2+ , it binds to one of two MerR binding sites forming a complex that acts as an activator of mer operon transcription [15]. Mermediated approaches have had broad applications in the bioremediation of mercury-contaminated environments and industrial waste streams [8,11,12,16,17].…”

Cloning of merA Gene from Methylotenera Mobilis for Mercury Biotransformation

“…The exposure of microbes to extreme conditions enforces the microbes to survive through genetic modifications [10,11]. Few microbes have developed a unique way to tolerate high concentration of mercury [12,13] by possessing the clustered genes in mer operon, located in the plasmids [14]. Amongst various genes in the operon, merA gene encodes for mercury reductase enzyme which breaks down inorganic form of mercury (Hg 2? )…”