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Extreme zinc tolerance in acidophilic microorganisms from the bacterial and archaeal domains

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Abstract

Zinc can occur in extremely high concentrations in acidic, heavy metal polluted environments inhabited by acidophilic prokaryotes. Although these organisms are able to thrive in such severely contaminated ecosystems their resistance mechanisms have not been well studied. Bioinformatic analysis of a range of acidophilic bacterial and archaeal genomes identified homologues of several known zinc homeostasis systems. These included primary and secondary transporters, such as the primary heavy metal exporter ZntA and Nramp super-family secondary importer MntH. Three acidophilic model microorganisms, the archaeon ‘Ferroplasma acidarmanus’, the Gram negative bacterium Acidithiobacillus caldus, and the Gram positive bacterium Acidimicrobium ferrooxidans, were selected for detailed analyses. Zinc speciation modeling of the growth media demonstrated that a large fraction of the free metal ion is complexed, potentially affecting its toxicity. Indeed, many of the putative zinc homeostasis genes were constitutively expressed and with the exception of ‘F. acidarmanus’ ZntA, they were not up-regulated in the presence of excess zinc. Proteomic analysis revealed that zinc played a role in oxidative stress in At. caldus and Am. ferrooxidans. Furthermore, ‘F. acidarmanus’ kept a constant level of intracellular zinc over all conditions tested whereas the intracellular levels increased with increasing zinc exposure in the remaining organisms.

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Acknowledgments

The authors acknowledge Caroline Ödling for her initial work on the bioinformatic predictions of zinc transporters, Siv Sääf for carrying out growth experiments, and Maria Liljeqvist for discussions and critical reading of the manuscript. This project was funded by the Swedish Research Council (Vetenskapsrådet contract number 621-2007-3537).

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  1. Joanna Potrykus

    Present address: Aberdeen Fungal Group, University of Aberdeen, Scotland, UK

Authors and Affiliations

  1. Molecular Biology, Umeå University, SE-901 87, Umeå, Sweden

    Stefanie Mangold, Joanna Potrykus & Mark Dopson

  2. Department of Chemistry, Umeå University, Umeå, Sweden

    Erik Björn & Lars Lövgren

  3. Centre for Ecology and Evolution in Microbial Model Systems, School of Natural Sciences, Linnaeus University, Kalmar, Sweden

    Mark Dopson

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  1. Stefanie Mangold
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Correspondence to Stefanie Mangold.

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Communicated by M. da Costa.

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Mangold, S., Potrykus, J., Björn, E. et al. Extreme zinc tolerance in acidophilic microorganisms from the bacterial and archaeal domains. Extremophiles 17, 75–85 (2013). https://doi.org/10.1007/s00792-012-0495-3

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