The ATPases CopA and CopB both contribute to copper resistance of the thermoacidophilic archaeon Sulfolobus solfataricus

Völlmecke, Christian; Drees, Steffen L.; Reimann, Julia; Albers, Sonja‐Verena; Lübben, Mathias

doi:10.1099/mic.0.055905-0

Cited by 45 publications

(35 citation statements)

References 57 publications

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“…Resistance to copper in extreme thermoacidophiles is mediated at least by mechanisms involving active transport and metal sequestration (7,(10)(11)(12)(13)(14)(15). Single-unit, membrane class 1B metal-translocating P-type ATPases are implicated in homeostasis and resistance to Cu 2ϩ and Cu ϩ , as well as to Ag ϩ , Pb 2ϩ , Zn 2ϩ , Cd 2ϩ , and Co 2ϩ (16).…”

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confidence: 99%

Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses

Wheaton

Mukherjee

Kelly

2016

Appl Environ Microbiol

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The extremely thermoacidophilic archaeon Metallosphaera sedula mobilizes metals by novel membrane-associated oxidase clusters and, consequently, requires metal resistance strategies. This issue was examined by "shocking" M. sedula with representative metals ( ORFs that responded to at least four metals, and 10 of these responded to all five metals. This core transcriptome indicated induction of Fe-S cluster assembly (Msed_1656-Msed_1657), tungsten/molybdenum transport (Msed_1780-Msed_1781), and decreased central metabolism. Not surprisingly, a metal-translocating P-type ATPase (Msed_0490) associated with a copper resistance system (Cop) was upregulated in response to Cu 2؉ (6-fold) but also in response to UO 2 2؉ (4-fold) and Zn 2؉ (9-fold). Cu 2؉ challenge uniquely induced assimilatory sulfur metabolism for cysteine biosynthesis, suggesting a role for this amino acid in Cu 2؉ resistance or issues in sulfur metabolism. The results indicate that M. sedula employs a range of physiological and biochemical responses to metal challenge, many of which are specific to a single metal and involve proteins with yet unassigned or definitive functions. IMPORTANCEThe mechanisms by which extremely thermoacidophilic archaea resist and are negatively impacted by metals encountered in their natural environments are important to understand so that technologies such as bioleaching, which leverage microbially based conversion of insoluble metal sulfides to soluble species, can be improved. Transcriptomic analysis of the cellular response to metal challenge provided both global and specific insights into how these novel microorganisms negotiate metal toxicity in natural and technological settings. As genetics tools are further developed and implemented for extreme thermoacidophiles, information about metal toxicity and resistance can be leveraged to create metabolically engineered strains with improved bioleaching characteristics. E xtremely thermoacidophilic archaea from the genera Sulfolobus, Acidianus, and Metallosphaera can inhabit natural and anthropogenic environments laden with metals (1) and, as a consequence, require strategies to avert the deleterious impact of these metals on cellular function (2). For some species within the Sulfolobales, metal oxidation mediated by membrane-bound, oxidase clusters provides a cellular bioenergetic benefit (3-5). However, at the same time, utilization of this energy source contributes to the toxicity of the biotope by mobilizing metal cations that can subsequently inhibit biological function (6, 7). As a consequence, the interconnections between metal biooxidation, toxicity, and resistance are important to consider to have a full appreciation of how these unique microorganisms survive in extreme environments (8).For extremely thermoacidophilic archaea, the most studied metal thus far has been copper, because of its importance in biohydrometallurgy (9). Resistance to copper in extreme thermoacidophiles is mediated at least by mechanisms involving active transport and metal sequestr...

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Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses

Wheaton

Mukherjee

Kelly

2016

Appl Environ Microbiol

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“…Among the best-studied P-type ATPases are the Na ϩ /K ϩ pump (44,54), the plasma membrane H ϩ pump (48), and the Ca 2ϩ -ATPase (the P IIA group) (63,64), commonly found in eukaryotic cells but also present in some prokaryotes (21). Structures of several P-type ATPases have been determined by X-ray crystallography (28,44,48,54,62 (42,50,58,66). The P IB -ATPases include the two human Cu ϩ -ATPases in which mutations are responsible for Menkes and Wilson diseases (17).…”

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Characterization of the P _IB -Type ATPases Present in Thermus thermophilus

Schurig-Briccio

Gennis

2012

J Bacteriol

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“…While the M. sedula copRTA locus conferred copper resistance when expressed in S. solfataricus, the level produced was more than 8-fold less than the resistance level of wild-type M. sedula (76 mM). This suggested that there are additional factors controlling metal resistance that are native to M. sedula, such as copB (9,47) and ppx (36). To better understand the importance of copA, it was necessary to develop a genetic system in M. sedula, and this was pursued in part because cross-species gene expression was successful.…”

Section: Resultsmentioning

confidence: 99%

“…Many archaeal genomes contain copA (P-type ATPase) copper efflux transporters, with the most well-characterized example being found in the hyperthermophilic sulfate reducer Archaeoglobus fulgidis (1, 13). Multiple mechanisms of copper resistance also have been identified in Sulfolobus solfataricus, including a copper efflux system consisting of copA and copB (Ptype ATPase), copR (regulator), and copT (metallochaperone) (9,11,46,47). An inorganic polyphosphate symport system identified in the related Sulfolobus metallicus has also been predicted to play a critical role in copper resistance (36).…”

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Metal Resistance and Lithoautotrophy in the Extreme Thermoacidophile Metallosphaera sedula

et al. 2012

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Archaea such as Metallosphaera sedula are thermophilic lithoautotrophs that occupy unusually acidic and metal-rich environments. These traits are thought to underlie their industrial importance for bioleaching of base and precious metals. In this study, a genetic approach was taken to investigate the specific relationship between metal resistance and lithoautotrophy during biotransformation of the primary copper ore, chalcopyrite (CuFeS 2 ). In this study, a genetic system was developed for M. sedula to investigate parameters that limit bioleaching of chalcopyrite. The functional role of the M. sedula copRTA operon was demonstrated by cross-species complementation of a copper-sensitive Sulfolobus solfataricus copR mutant. Inactivation of the gene encoding the M. sedula copper efflux protein, copA, using targeted recombination compromised metal resistance and eliminated chalcopyrite bioleaching. In contrast, a spontaneous M. sedula mutant (CuR1) with elevated metal resistance transformed chalcopyrite at an accelerated rate without affecting chemoheterotrophic growth. Proteomic analysis of CuR1 identified pleiotropic changes, including altered abundance of transport proteins having AAA-ATPase motifs. Addition of the insoluble carbonate mineral witherite (BaCO 3 ) further stimulated chalcopyrite lithotrophy, indicating that carbon was a limiting factor. Since both mineral types were actively colonized, enhanced metal leaching may arise from the cooperative exchange of energy and carbon between surface-adhered populations. Genetic approaches provide a new means of improving the efficiency of metal bioleaching by enhancing the mechanistic understanding of thermophilic lithoautotrophy.N early 80% of current global copper reserves are comprised of low-quality metal ores (10,25,44). Consequently, the need for cost-efficient extraction methods has promoted interest in the use of microbe-based processing. Bioleaching is an established approach for the extraction of base and precious metals from sulfidic ores (30,34,35,43). Bioleaching using thermophilic microbes is of particular importance for certain metals. In the case of copper, elevated temperatures produced naturally in heaps overcome recalcitrant extraction due to surface passivation while chemical reaction rates are accelerated (29,30). A critical disadvantage of bioleaching is the amount of time required for metal solubilization, often spanning years (22,38). Therefore, improved metal recovery must include factors that accelerate this process, particularly those inspired by biotechnologic approaches (48).Thermoacidophilic archaea include taxa that are lithoautotrophic and unusually metal resistant (3,19). These organisms are native to pyritic or sulfur-rich geothermal habitats and are used to recover base and precious metals from low-quality sulfidic minerals through bioleaching processes (31). In the bioleaching process, both direct and indirect leaching mechanisms have been proposed that convert metals to soluble forms (33, 40). Metal release may occur via metab...

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The ATPases CopA and CopB both contribute to copper resistance of the thermoacidophilic archaeon Sulfolobus solfataricus

Cited by 45 publications

References 57 publications

Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses

Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses

Characterization of the P _IB -Type ATPases Present in Thermus thermophilus

Metal Resistance and Lithoautotrophy in the Extreme Thermoacidophile Metallosphaera sedula

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The ATPases CopA and CopB both contribute to copper resistance of the thermoacidophilic archaeon Sulfolobus solfataricus

Cited by 45 publications

References 57 publications

Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses

Transcriptomes of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Exposed to Metal “Shock” Reveal Generic and Specific Metal Responses

Characterization of the P IB -Type ATPases Present in Thermus thermophilus

Metal Resistance and Lithoautotrophy in the Extreme Thermoacidophile Metallosphaera sedula

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Characterization of the P _IB -Type ATPases Present in Thermus thermophilus