Heavy Metal Resistance Strategies of Acidophilic Bacteria and Their Acquisition: Importance for Biomining and Bioremediation

Abstract

Microbial solubilizing of metals in acid environments is successfully used in industrial bioleaching of ores or biomining to extract metals such as copper, gold, uranium and others. This is done mainly by acidophilic and other microorganisms that mobilize metals and generate acid mine drainage or AMD, causing serious environmental problems. However, bioremediation or removal of the toxic metals from contaminated soils can be achieved by using the specifi c properties of the acidophilic microorganisms interacting with these elements. These bacteria resist high levels of metals by using a few "canonical" systems such as active effl ux or trapping of the metal ions by metal chaperones. Nonetheless, gene duplications, the presence of genomic islands, the existence of additional mechanisms such as passive instruments for pH and cation homeostasis in acidophiles and an inorganic polyphosphate-driven metal resistance mechanism have also been proposed. Horizontal gene transfer in environmental microorganisms present in natural ecosystems is considered to be an important mechanism in their adaptive evolution. This process is carried out by diff erent mobile genetic elements, including genomic islands (GI), which increase the adaptability and versatility of the microorganism. This mini-review also describes the possible role of GIs in metal resistance of some environmental microorganisms of importance in biomining and bioremediation of metal polluted environments such as Thiomonas arsenitoxydans, a moderate acidophilic microorganism, Acidithiobacillus caldus and Acidithiobacillus ferrooxidans strains ATCC 23270 and ATCC 53993, all extreme acidophiles able to tolerate exceptionally high levels of heavy metals. Some of these bacteria contain variable numbers of GIs, most of which code for high numbers of genes related to metal resistance. In some cases there is an apparent correlation between the number of metal resistance genes and the metal tolerance of each of these microorganisms. It is expected that a detailed knowledge of the mechanisms that these environmental microorganisms use to adapt to their harsh niche will help to improve biomining and metal bioremediation in industrial processes.

Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’

“…Although the role of HGT in conferring specific capabilities to recipient prokaryotic species, for example, antibiotic resistance or heavy metal resistance (Andam et al, 2011;Navarro et al, 2013), has long been recognized, the impact of HGT on prokaryotic evolutionary history and its potential role in organismal transition to new habitats and lifestyles has received less attention. The acquisition of bacterial genes was recently proposed as a driver of Halobacteriales evolution from a methanogenic ancestor (Nelson-Sathi et al, 2012).…”

The Confluence of Heavy Metal Biooxidation and Heavy Metal Resistance: Implications for Bioleaching by Extreme Thermoacidophiles

“…The following section describes the current knowledge of metal resistance mechanisms with an emphasis on extremely thermoacidophilic microorganisms, useful for bioleaching applications. Comprehensive reviews covering microbial metal resistance exist, but few specifically target extreme thermoacidophiles [141][142][143][144][145][146]. …”

“…The role of polyP in metal resistance in extremophiles encompasses both its role as an energy source and metal chelating agent. Through the action of PPX, the microorganism can generate organic phosphate for metal chelation, or the reversible reaction catalyzed by PPK can generate additional ATP for heavy-metal efflux systems or other cellular metabolism associated with metal challenge [142]. The importance of phosphate metabolism, specifically import via an archaeal Pit system, to enhanced copper resistance for an M. sedula mutant has been established and indicates phosphate plays a key role in supernormal copper resistance [157].…”

Toxic metal resistance in biofilms: diversity of microbial responses and their evolution

“…A comparative study on several metagenomics data suggest that microorganisms found in extreme environments evolve faster, and the frequency of HGT is higher, than in those found in non-extreme environment[81]. Interestingly, an enrichment in genes involved in recombination, replication and DNA repair was observed in the genomes of microorganisms found in AMDs, and in particular in the biofilms of the Richmond mine[81], and genomic islands carrying metal resistance genes have been detected in several bacteria capable of forming biofilms which may have been acquired by HGT processes [33,[82][83][84].All these data suggest that toxic metals may favor mutation occurrence, HGT and thus accelerate evolution of such microorganisms. To date, only one study was performed in Tm.sp.…”