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Metallosphaera Sedula Provides Insights Into Bioleaching-Associated Metabolism Kathryne S

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Metallosphaera Sedula Provides Insights Into Bioleaching-Associated Metabolism Kathryne S University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in the Biological Sciences Papers in the Biological Sciences 2008 The Genome Sequence of the Metal-Mobilizing, Extremely Thermoacidophilic Archaeon Metallosphaera sedula Provides Insights into Bioleaching-Associated Metabolism Kathryne S. Auernik North Carolina State University Yukari Maezato University of Nebraska-Lincoln Paul H. Blum University of Nebraska - Lincoln, [email protected] Robert M. Kelly North Carolina State University Follow this and additional works at: http://digitalcommons.unl.edu/bioscifacpub Part of the Biology Commons Auernik, Kathryne S.; Maezato, Yukari; Blum, Paul H.; and Kelly, Robert M., "The Genome Sequence of the Metal-Mobilizing, Extremely Thermoacidophilic Archaeon Metallosphaera sedula Provides Insights into Bioleaching-Associated Metabolism" (2008). Faculty Publications in the Biological Sciences. 517. http://digitalcommons.unl.edu/bioscifacpub/517 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in the Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Feb. 2008, p. 682–692 Supporting information for Vol. 74, No. 3 0099-2240/08/$08.00ϩ0 doi:10.1128/AEM.02019-07 this article is available Copyright © 2008, American Society for Microbiology. All Rights Reserved. following the references. The Genome Sequence of the Metal-Mobilizing, Extremely Thermoacidophilic Archaeon Metallosphaera sedula Provides Insights into Bioleaching-Associated Metabolismᰔ† Kathryne S. Auernik,1 Yukari Maezato,2 Paul H. Blum,2 and Robert M. Kelly1* Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, North Carolina 27695-7905,1 and Beadle Center for Genetics, University of Nebraska—Lincoln, Lincoln, Nebraska 68588-066622 Received 4 September 2007/Accepted 1 December 2007 Despite their taxonomic description, not all members of the order Sulfolobales are capable of oxidizing reduced sulfur species, which, in addition to iron oxidation, is a desirable trait of biomining microorganisms. However, the complete genome sequence of the extremely thermoacidophilic archaeon Metallosphaera sedula DSM 5348 (2.2 Mb, ϳ2,300 open reading frames [ORFs]) provides insights into biologically catalyzed metal sulfide oxidation. Comparative genomics was used to identify pathways and proteins involved (directly or indirectly) with bioleaching. As expected, the M. sedula genome contains genes related to autotrophic carbon fixation, metal tolerance, and adhesion. Also, terminal oxidase cluster organization indicates the presence of hybrid quinol-cytochrome oxidase complexes. Comparisons with the mesophilic biomining bacterium Acidi- thiobacillus ferrooxidans ATCC 23270 indicate that the M. sedula genome encodes at least one putative rusti- cyanin, involved in iron oxidation, and a putative tetrathionate hydrolase, implicated in sulfur oxidation. The fox gene cluster, involved in iron oxidation in the thermoacidophilic archaeon Sulfolobus metallicus, was also identified. These iron- and sulfur-oxidizing components are missing from genomes of nonleaching members of the Sulfolobales, such as Sulfolobus solfataricus P2 and Sulfolobus acidocaldarius DSM 639. Whole-genome transcriptional response analysis showed that 88 ORFs were up-regulated twofold or more in M. sedula upon addition of ferrous sulfate to yeast extract-based medium; these included genes for components of terminal oxidase clusters predicted to be involved with iron oxidation, as well as genes predicted to be involved with sulfur metabolism. Many hypothetical proteins were also differentially transcribed, indicating that aspects of the iron and sulfur metabolism of M. sedula remain to be identified and characterized. Biomining exploits acidophilic microorganisms to recover 59). As accumulation of precipitating RISC compounds can valuable metals (i.e., Cu and Au) from ores ( 52, 56, 57, 59) in slow leaching rates (52), microbial RISC-oxidizing capabilities biohydrometallurgical processes conducted at temperatures are beneficial. Extreme thermophiles are particularly desir- ranging from ambient ( 44, 71 ) to 80°C (17). Higher-temper- able, as problematic passivation on ore surfaces decreases at ature operations involve consortia of extremely thermoacido- higher temperatures. Since chemolithotrophs use Fe(II) philic archaea from the genera Sulfolobus, Acidianus, and and/or RISCs as energy sources, nutritional supplement costs Metallosphaera (49, 50). For example, Sulfolobus metallicus, are relatively low, thus minimizing process economic impact. certain Acidianus species ( 12, 47 ), and Metallosphaera sedula Components of electron transport chains involved in Fe and (29, 33) all can mobilize metals from metal sulfides. However, RISC oxidation are differentially expressed as a function of not all members of these genera are metal bioleachers. In fact, substrate in both meso- and thermoacidophilic bioleachers (5, the three Sulfolobus species with completed genome sequences 36, 55). Bacterial Fe oxidation studies focused on mesophilic (S. solfataricus, S. acidocaldarius, and S. tokodaii) are appar- A. ferrooxidans have shown that electrons from Fe(II) can be ently unable to effect metal sulfide oxidation. Since genome transported along either a “downhill” or an “uphill” electron sequences are not yet available for metal- bioleaching extreme ϩ pathway, towards a lower (O2/H2O)- or higher [NAD(P) / thermoacidophiles, genetic features characteristic of this phys- NAD(P)H]-potential redox couple, respectively (28). Both iological capability remain to be seen. pathways involve electron transfer via cytochromes c and rus- Biomining is based upon biological oxidation of iron (Fe) ticyanin (Rus), a periplasmic blue copper protein (Bcp). The and reduced inorganic sulfur compounds (RISCs). Two downhill and uphill pathways, encoded by the rus and petI Fe(III)-driven chemical leaching mechanisms are catalyzed by operons, conclude with reduction of the final target by a cyto- microorganisms regenerating Fe(III) from Fe(II), facilitating chrome c oxidase (CoxABCD) and bc complex (PetI), respec- release of valuable metals bound in metal sulfides (52, 56, 57, 1 tively, and are highly transcribed on Fe(II) relative to elemen- tal sulfur (S0) (7, 18, 72). In a proposed archaeal Fe oxidation * Corresponding author. Mailing address: Department of Chemical model, based on Ferroplasma strains, the terminal oxidase & Biomolecular Engineering, North Carolina State University, Ra- combines select bc1 complex-like and cytochrome c oxidase- leigh, NC 27695-7905. Phone: (919) 515-6396. Fax: (919) 515-3465. like components and involves association of a Bcp, sulfocyanin E-mail: [email protected]. (15). Aspects of this model were noted previously in the non- † Supplemental material for this article may be found at http://aem .asm.org/. leacher S. acidocaldarius (39, 41), while a correlation between ᰔ Published ahead of print on 14 December 2007. cytochromes b, b558/562 (CbsAB), and Fe-S cluster proteins 682 VOL. 74, 2008 METALLOSPHAERA SEDULA GENOME SEQUENCE 683 (possible quinol oxidase components) and the bc1 complex has have been implicated in adhesion (46, 66), and pilus-like struc- been proposed (27, 39, 65, 75). Finally, a gene cluster contain- tures, along with “wiggling of the cells at the ore,” were ob- ing terminal oxidase and electron transport chain components, served during initial characterization of M. sedula (29). highly transcribed on Fe(II) versus S0, was identified in S. To better understand the defining features of extreme ther- metallicus (5). moacidophiles capable of metal sulfide oxidation, the genome Extremely thermoacidophilic archaeal RISC oxidation sequence of M. sedula was completed and probed for clues with mechanisms have not been established. RISC electrons may respect to five physiological areas (iron oxidation, sulfur oxi- enter the electron transport chain via a membrane-bound thio- dation, carbon fixation, metal toxicity, and adhesion) that are 2Ϫ sulfate (S2O3 ):quinone oxidoreductase (TQO), a sulfite: important to its current and future role in biomining opera- acceptor oxidoreductase, or possibly a sulfide:quinone oxi- tions. In addition, whole-genome transcriptional response doreductase (38). Despite the annotation, tetrathionate hydro- analysis was used to identify specific open reading frames 0 2Ϫ lases (TetH) expressed on S , FeS2, and S2O3 substrates (ORFs) related to Fe oxidation. have been noted in A. ferrooxidans and Acidithiobacillus caldus (8, 35, 61). Certain terminal oxidase components have been expressed in extremely thermoacidophilic archaea grown on MATERIALS AND METHODS specific RISCs (36, 54). Although not directly linked to elec- Sequencing of the M. sedula genome. M. sedula (DSM 5348T) was purified to tron transport, sulfur oxygenase reductases (Sor) are believed clonality by aerobic cultivation at 70°C on a solid medium, prepared as described to be important for breakdown of intracellular RISCs, partic- previously (64), and adjusted to a pH of 2.5 with sulfuric acid. High-molecular- ularly S0 or polysulfides (11, 37, 69). M. sedula growth on S0 weight genomic DNA was isolated, as described previously (26), and provided to the U.S. Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/)
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