The genus Metallosphaera contains extremely thermoacidophilic (Topt ≥ 65°C, pHopt ≤ 3.5) archaea capable of mobilizing heavy metals from sulfidic ores for bioenergetic needs via a repertoire of novel membrane-associated oxidase clusters. The capacity makes certain members of the genus suitable biocatalysts for the biomining of base, precious and strategic metals from ore bodies. However, the mobilization of heavy metals creates a unique and dynamic equilibrium between bioenergetics needs and mechanisms for tolerating/resisting the toxic effects imposed by solubilized metal species (Wheaton et al., Minerals 5:39-451, 2015). The resistance aspect was examined for M. sedula by ‘shocking’ this archaeon at non-toxic and toxic levels with copper, zinc, nickel, uranium, or cobalt, all heavy metals associated with mining environments. The vast majority of ORFs responded to only one metal at non-toxic and toxic levels, indicating metal-specific strategies to heavy metal challenge as well as unique modes of toxicity. Related work comparing two nearly identical Metallosphaera species, one isolated from a solfatara (M. sedula) and the second from an abandoned uranium mine (M. prunae), revealed variations in the capacity for mobilization and resistance to uranium (Mukherjee, Wheaton et al., PNAS 109:16702-16707, 2012). The difference in mobilization was attributed to a mutation in the ferrous iron oxidation (Fox) cluster, while differences in resistance indicated involvement of toxin-antitoxin loci. Continued work comparing the two species revealed both are capable of mobilizing vanadium and molybdenum oxides, suggesting a novel biooxidation mechanism beyond the suspected Fox cluster. Taken together this work (1) supports the notion of the capacity for metal mobilization being inherently coupled to the ability to resist solubilized metal species, and (2) expands the repertoire of biooxidation substrates beyond sulfidic ores. The results provide a basis for designing novel metal mobilization applications, which are appropriately engineered to incorporate the capacity/resistance interplay.

Extreme thermoacidophiles as biocatalysts for heavy metal recovery: A delicate balance between biooxidation and resistance

251st National Meeting (2016)

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