[go: up one dir, main page]
Skip to main content

Advertisement

Springer Nature Link
Log in

Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

This mini-review describes the current status of recent genome sequencing projects of extremely acidophilic microorganisms and highlights the most current scientific advances emerging from their analysis. There are now at least 56 draft or completely sequenced genomes of acidophiles including 30 bacteria and 26 archaea. There are also complete sequences for 38 plasmids, 29 viruses, and additional DNA sequence information of acidic environments is available from eight metagenomic projects. A special focus is provided on the genomics of acidophiles from industrial bioleaching operations. It is shown how this initial information provides a rich intellectual resource for microbiologists that has potential to open innovative and efficient research avenues. Examples presented illustrate the use of genomic information to construct preliminary models of metabolism of individual microorganisms. Most importantly, access to multiple genomes allows the prediction of metabolic and genetic interactions between members of the bioleaching microbial community (ecophysiology) and the investigation of major evolutionary trends that shape genome architecture and evolution. Despite these promising beginnings, a major conclusion is that the genome projects help focus attention on the tremendous effort still required to understand the biological principles that support life in extremely acidic environments, including those that might allow engineers to take appropriate action designed to improve the efficiency and rate of bioleaching and to protect the environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allen EE, Banfield JF (2005) Community genomics in microbial ecology and evolution. Nat Rev Micro 3:489–498

    Article  CAS  Google Scholar 

  • Allen EE, Tyson GW, Whitaker RJ, Detter JC, Richardson PM, Banfield JF (2007) Genome dynamics in a natural archaeal population. Proc Natl Acad Sci 104:1883–1888

    Article  CAS  Google Scholar 

  • Amouric A, Appia-Ayme C, Yarzabal A, Bonnefoy V (2009) Regulation of the iron and sulfur oxidation pathways in the acidophilic Acidithiobacillus ferrooxidans. Adv Mater Res 71–73:163–166

    Article  Google Scholar 

  • Andersson AF, Banfield JF (2008) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:1047–1050

    Article  CAS  Google Scholar 

  • Appia-Ayme C, Quatrini R, Denis Y, Denizot F, Silver S, Roberto F, Veloso F, Valdés J, Pablo Cárdenas J, Esparza M, Orellana O, Jedlicki E, Bonnefoy V, Holmes DS (2006) Microarray and bioinformatic analyses suggest models for carbon metabolism in the autotroph Acidithiobacillus ferrooxidans. Hydrometallurgy 83:273–280

    Article  CAS  Google Scholar 

  • Arsène-Ploetze F, Koechler S, Marchal M, Coppée J-Y, Chandler M, Bonnefoy V, Brochier-Armanet C, Barakat M, Barbe V, Battaglia-Brunet F, Bruneel O, Bryan CG, Cleiss-Arnold J, Cruveiller S, Erhardt M, Heinrich-Salmeron A, Hommais F, Joulian C, Krin E, Lieutaud A, Lièvremont D, Michel C, Muller D, Ortet P, Proux C, Siguier P, Roche D, Rouy Z, Salvignol G, Slyemi D, Talla E, Weiss S, Weissenbach J, Médigue C, Bertin PN (2010) Structure, function, and evolution of the thiomonas spp. Genome. PLoS Genet 6:e1000859

    Article  CAS  Google Scholar 

  • Auernik KS, Maezato Y, Blum PH, Kelly RM (2008) The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl Environ Microbiol 74:682–692

    Article  CAS  Google Scholar 

  • Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    Article  CAS  Google Scholar 

  • Baker BJ, Tyson GW, Goosherst L, Banfield JF (2009) Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Appl Environ Microbiol 75:2192–2199

    Article  CAS  Google Scholar 

  • Baker BJ, Comolli LR, Dick GJ, Hauser LJ, Hyatt D, Dill BD, Land ML, VerBerkmoes NC, Hettich RL, Banfield JF (2010) Enigmatic, ultrasmall, uncultivated Archaea. Proc Natl Acad Sci 107:8806–8811

    Article  CAS  Google Scholar 

  • Baker-Austin C, Dopson M, Wexler M, Sawers RG, Bond PL (2005) Molecular insight into extreme copper resistance in the extremophilic archaeon ‘Ferroplasma acidarmanus’ Fer1. Microbiology 151:2637–2646

    Article  CAS  Google Scholar 

  • Barreto M, Quatrini R, Bueno S, Arriagada C, Valdes J, Silver S, Jedlicki E, Holmes DS (2003) Aspects of the predicted physiology of Acidithiobacillus ferrooxidans deduced from an analysis of its partial genome sequence. Hydrometallurgy 71:97–105

    Article  CAS  Google Scholar 

  • Barreto M, Gehrke T, Harneit K, Sand W, Jedlicki E, Holmes D (2005a) Unexpected insights into biofilm formation by Acidithiobacillus ferrooxidans revealed by genome analysis and experimental approaches. In: Harrison S, Rawlings D, Peterson J (eds) 16th International Biohydrometallurgy Symposium. Cape Town, South Africa, pp 817–825

    Google Scholar 

  • Barreto M, Jedlicki E, Holmes DS (2005b) Identification of a gene cluster for the formation of extracellular polysaccharide precursors in the chemolithoautotroph Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:2902–2909

    Article  CAS  Google Scholar 

  • Berg IA, Kockelkorn D, Ramos-Vera WH, Say RF, Zarzycki J, Hügler M, Alber BE, Fuchs G (2010a) Autotrophic carbon fixation in archaea. Nat Rev Micro 8:447–460

    Article  CAS  Google Scholar 

  • Berg IA, Ramos-Vera WH, Petri A, Huber H, Fuchs G (2010b) Study of the distribution of autotrophic CO2 fixation cycles in Crenarchaeota. Microbiology 156:256–269

    Article  CAS  Google Scholar 

  • Bonnefoy V (2010) Bioinformatics and genomics of iron and sulfur oxidizing acidophiles. In: Barton L, Mandl M, Loy A (eds) Geomicrobiology: molecular and environmental perspective

  • Bouchal P, Zdráhal Z, Helánová S, Janiczek O, Hallberg KB, Mandl M (2006) Proteomic and bioinformatic analysis of iron- and sulfur-oxidizing Acidithiobacillus ferrooxidans using immobilized pH gradients and mass spectrometry. Proteomics 6:4278–4285

    Article  CAS  Google Scholar 

  • Brügger K, Torarinsson E, Redder P, Chen L, Garrett RA (2004) Shuffling of Sulfolobus genomes by autonomous and non-autonomous mobile elements. Biochem Soc Trans 32:179–183

    Article  Google Scholar 

  • Cabrejos M-E, Zhao H-L, Guacucano M, Bueno S, Levican G, Garcia E, Jedlicki E, Holmes DS (1999) IST1 insertional inactivation of the resB gene: implications for phenotypic switching in Thiobacillus ferrooxidans. FEMS Microbiol Lett 175:223–229

    Article  CAS  Google Scholar 

  • Castro M, Ruiz L, Díaz M, Mamani S, Jerez CA, Holmes DS, Guiliani N (2009) C-Di-GMP pathway in biomining bacteria. Adv Mater Res 71–73:223–226

    Article  Google Scholar 

  • Chen L, Brugger K, Skovgaard M, Redder P, She Q, Torarinsson E, Greve B, Awayez M, Zibat A, Klenk H-P, Garrett RA (2005) The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187:4992–4999

    Article  CAS  Google Scholar 

  • Chi A, Valenzuela L, Beard S, Mackey AJ, Shabanowitz J, Hunt DF, Jerez CA (2007) Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans. Mol Cell Proteomics 6:2239–2251

    Article  CAS  Google Scholar 

  • Cid C, Garcia-Descalzo L, Casado-Lafuente V, Amils R, Aguilera A (2010) Proteomic analysis of the response of an acidophilic strain of Chlamydomonas sp. (Chlorophyta) to natural metal-rich water. Proteomics 10(10):2026–2036

    Article  CAS  Google Scholar 

  • Clennel A, Johnston B, Rawlings D (1995) Structure and function of Tn5467, a Tn21-like transposon located on the Thiobacillus ferrooxidans broad-host-range plasmid pTF-FC2. Appl Environ Microbiol 61:4223–4229

    CAS  Google Scholar 

  • Clum A, Nolan M, Lang E, Rio TGD, Tice H, Copeland A, Cheng J-F, Lucas S, Chen F, Bruce D, Goodwin L, Pitluck S, Ivanova N, Mavromatis K, Mikhailova N, Pati A, Chen A, Palaniappan K, Göker M, Spring S, Land M, Hauser L, Chang Y-J, Jeffries CD, Chain P, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk H-P, Lapidus A (2009) Complete genome sequence of Acidimicrobium ferrooxidans type strain (ICPT). Standards in Genomic Sciences

  • Demergasso CS, Galleguillos F, Soto P, Serón M, Iturriaga V (2010) Microbial succession during a heap bioleaching cycle of low grade copper sulfides. Does this knowledge mean a real input for industrial process design and control? Hydrometallurgy

  • Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ, Thomas BC, VerBerkmoes NC, Hettich RL, Banfield JF (2010a) Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci 107:2383–2390

    Article  CAS  Google Scholar 

  • Denef VJ, Mueller RS, Banfield JF (2010b) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4:599–610

    Article  Google Scholar 

  • Dick G, Andersson A, Baker B, Simmons S, Thomas B, Yelton AP, Banfield J (2009) Community-wide analysis of microbial genome sequence signatures. Genome Biol 10:R85

    Article  CAS  Google Scholar 

  • Dopson M (2010) Ecology, adaptations, and applications of acidophiles. In: R A (ed) Extremophiles: microbiology and biotechnology. Horizon Press

  • Duarte F, Araya-Secchi R, González W, Perez-Acle T, González-Nilo D, Holmes DS (2009) Protein function in extremely acidic conditions: molecular simulation studies of a predicted aquaporin and a voltage gated potassium channel in Acidithiobacillus ferrooxidans. Adv Mater Res 71–73:211–214

    Article  Google Scholar 

  • Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, deWinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138

    Article  CAS  Google Scholar 

  • Esparza M, Bowien B, Jedlicki E, Holmes DS (2009) Gene organization and CO2-responsive expression of four Cbb operons in Acidithiobacillus ferrooxidans. Adv Mater Res 71–73:207–210

    Article  Google Scholar 

  • Esparza M, Cardenas JP, Bowien B, Jedlicki E, Holmes DS (2010) CO2 fixation in the obligate, chemolithoautotrophic acidophile, Acidithiobacillus ferrooxidans. BMC Microbiology

  • Farah C, Vera M, Morin D, Haras D, Jerez CA, Guiliani N (2005) Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:7033–7040

    Article  CAS  Google Scholar 

  • Filee J, Siguier P, Chandler M (2007) Insertion sequence diversity in archaea. Microbiol Mol Biol Rev 71:121–157

    Article  CAS  Google Scholar 

  • Fütterer O, Angelov A, Liesegang H, Gottschalk G, Schleper C, Schepers B, Dock C, Antranikian G, Liebl W (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci USA 101:9091–9096

    Article  Google Scholar 

  • Garrido P, González-Toril E, García-Moyano A, Moreno-Paz M, Amils R, Parro V (2008) An oligonucleotide prokaryotic acidophile microarray: its validation and its use to monitor seasonal variations in extreme acidic environments with total environmental RNA. Environ Microbiol 10:836–850

    Article  CAS  Google Scholar 

  • Goltsman DSA, Denef VJ, Singer SW, VerBerkmoes NC, Lefsrud M, Mueller RS, Dick GJ, Sun CL, Wheeler KE, Zemla A, Baker BJ, Hauser L, Land M, Shah MB, Thelen MP, Hettich RL, Banfield JF (2009) Community genomic and proteomic analyses of chemoautotrophic iron-oxidizing “Leptospirillum rubarum” (Group II) and “Leptospirillum ferrodiazotrophum” (Group III) bacteria in acid mine drainage biofilms. Appl Environ Microbiol 75:4599–4615

    Article  CAS  Google Scholar 

  • Gonzalez-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69:4853–4865

    Article  CAS  Google Scholar 

  • González-Toril E, Aguilera A, Rodriguez N, Fernández-Remolar D, Gómez F, Diaz E, García-Moyano A, Sanz JL, Amils R (2010) Microbial ecology of Río Tinto, a natural extreme acidic environment of biohydrometallurgical interest. Hydrometallurgy (in press)

  • Hold C, Andrews BA, Asenjo JA (2009) A stoichiometric model of Acidithiobacillus ferrooxidans ATCC 23270 for metabolic flux analysis. Biotechnol Bioeng 102:1448–1459

    Article  CAS  Google Scholar 

  • Holmes DS, Bonnefoy V (2007) Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms. In: Rawlings DE, Johnson DB (eds) Biomining. Springer, Berlin, pp 281–307

    Chapter  Google Scholar 

  • Holmes DS, Barreto M, Valdes J, Dominguez C, Arriagada C, Silver S, Bueno S, Jedlicki E (2001) Genome sequence of Acidithiobacillus ferrooxidans: metabolic reconstruction, heavy metal resistance and other characteristics. In: Ciminelli V, Garcia O (eds) Biohydrometallurgy: fundamentals, technology and sustainable development. Elsevier, Amsterdam, pp 237–251

    Google Scholar 

  • Hou S, Makarova K, Saw J, Senin P, Ly B, Zhou Z, Ren Y, Wang J, Galperin M, Omelchenko M, Wolf Y, Yutin N, Koonin E, Stott M, Mountain B, Crowe M, Smirnova A, Dunfield P, Feng L, Wang L, Alam M (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26

    Article  CAS  Google Scholar 

  • Jerez CA (2008) The use of genomics, proteomics and other OMICS technologies for the global understanding of biomining microorganisms. Hydrometallurgy 94:162–169

    Article  CAS  Google Scholar 

  • Johnson DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27:307–317

    Article  CAS  Google Scholar 

  • Johnson DB (2008) Biodiversity and interactions of acidophiles: key to understanding and optimizing microbial processing of ores and concentrates. Trans Nonferrous Met Soc China 18:1367–1373

    Article  CAS  Google Scholar 

  • Kanao T, Matsumoto C, Shiraga K, Yoshida K, Takada J, Kamimura K (2010) Recombinant tetrathionate hydrolase from Acidithiobacillus ferrooxidans requires exposure to acidic conditions for proper folding. FEMS Microbiol Lett 309:43–47

    CAS  Google Scholar 

  • Kawarabayasi Y, Hino Y, Horikawa H, Jin-no K, Takahashi M, Sekine M, S-i B, Ankai A, Kosugi H, Hosoyama A, Fukui S, Nagai Y, Nishijima K, Otsuka R, Nakazawa H, Takamiya M, Kato Y, Yoshizawa T, Tanaka T, Kudoh Y, Yamazaki J, Kushida N, Oguchi A, K-i A, Masuda S, Yanagii M, Nishimura M, Yamagishi A, Oshima T, Kikuchi H (2001) Complete genome sequence of an aerobic thermoacidophilic Crenarchaeon, Sulfolobus tokodaii strain7. DNA Res 8:123–140

    Article  CAS  Google Scholar 

  • Kawashima T, Amano N, Koike H, S-i M, Higuchi S, Kawashima-Ohya Y, Watanabe K, Yamazaki M, Kanehori K, Kawamoto T, Nunoshiba T, Yamamoto Y, Aramaki H, Makino K, Suzuki M (2000) Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc Natl Acad Sci USA 97:14257–14262

    Article  CAS  Google Scholar 

  • Kondrat’eva T, Danilevich V, Ageeva S, Karavaiko G (2005) Identification of IS elements in Acidithiobacillus ferrooxidans strains grown in a medium with ferrous iron or adapted to elemental sulfur. Arch Microbiol 183:401–410

    Article  CAS  Google Scholar 

  • Kondrat’eva T, Danilevich V, Karavaiko G (2008) The primary structure and characteristics of the ISAfe600, an insertion sequence from Acidithiobacillus ferrooxidans strains. Mikrobiologiia 77:524–532

    Google Scholar 

  • Kotze AA, Tuffin IM, Deane SM, Rawlings DE (2006) Cloning and characterization of the chromosomal arsenic resistance genes from Acidithiobacillus caldus and enhanced arsenic resistance on conjugal transfer of ars genes located on transposon TnAtcArs. Microbiology 152:3551–3560

    Article  CAS  Google Scholar 

  • Levican G, Ugalde JA, Ehrenfeld N, Maass A, Parada P (2008) Comparative genomic analysis of carbon and nitrogen assimilation mechanisms in three indigenous bioleaching bacteria: predictions and validations. BMC Genomics 9:581

    Article  CAS  Google Scholar 

  • Levicán G, Katz A, Valdés J, Quatrini R, Holmes DS, Orellana O (2009) A 300 Kb genome segment, including a complete set of tRNA genes, is dispensable for Acidithiobacillus ferrooxidans. Adv Mater Res 71–73:187–190

    Article  Google Scholar 

  • Lipps G (2006) Plasmids and viruses of the thermoacidophilic crenarchaeote Sulfolobus. Extremophiles 10:17–28

    Article  Google Scholar 

  • Lo I, Denef VJ, VerBerkmoes NC, Shah MB, Goltsman D, DiBartolo G, Tyson GW, Allen EE, Ram RJ, Detter JC, Richardson P, Thelen MP, Hettich RL, Banfield JF (2007) Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446:537–541

    Article  CAS  Google Scholar 

  • Mueller RS, Denef VJ, Kalnejais LH, Suttle KB, Thomas BC, Wilmes P, Smith RL, Nordstrom DK, McCleskey RB, Shah MB, VerBerkmoes NC, Hettich RL, Banfield JF (2010) Ecological distribution and population physiology defined by proteomics in a natural microbial community. Mol Syst Biol 6

  • Navarro CA, Orellana LH, Mauriaca C, Jerez CA (2009) Transcriptional and functional studies of Acidithiobacillus ferrooxidans genes related to survival in the presence of copper. Appl Environ Microbiol 75:6102–6109

    Article  CAS  Google Scholar 

  • Oppon JC, Sarnovsky RJ, Craig NL, Rawlings DE (1998) A Tn7-like transposon is present in the glmUS region of the obligately chemoautolithotrophic bacterium Thiobacillus ferrooxidans. J Bacteriol 180:3007–3012

    CAS  Google Scholar 

  • Osorio H, Martinez V, Nieto P, Holmes D, Quatrini R (2008a) Microbial iron management mechanisms in extremely acidic environments: comparative genomics evidence for diversity and versatility. BMC Microbiol 8:203

    Article  CAS  Google Scholar 

  • Osorio H, Martínez V, Veloso FA, Pedroso I, Valdés J, Jedlicki E, Holmes DS, Quatrini R (2008b) Iron homeostasis strategies in acidophilic iron oxidizers: studies in Acidithiobacillus and Leptospirillum. Hydrometallurgy 94:175–179

    Article  CAS  Google Scholar 

  • Ozsolak F, Platt AR, Jones DR, Reifenberger JG, Sass LE, McInerney P, Thompson JF, Bowers J, Jarosz M, Milos PM (2009) Direct RNA sequencing. Nature 461:814–818

    Article  CAS  Google Scholar 

  • Parro V, Moreno-Paz M, González-Toril E (2007) Analysis of environmental transcriptomes by DNA microarrays. Environ Microbiol 9:453–464

    Article  CAS  Google Scholar 

  • Prangishvili D, Albers S-V, Holz I, Arnold HP, Stedman K, Klein T, Singh H, Hiort J, Schweier A, Kristjansson JK, Zillig W (1998) Conjugation in archaea: frequent occurrence of conjugative plasmids in sulfolobus. Plasmid 40:190–202

    Article  CAS  Google Scholar 

  • Prangishvili D, Stedman K, Zillig W (2001) Viruses of the extremely thermophilic archaeon Sulfolobus. Trends Microbiol 9:39–43

    Article  CAS  Google Scholar 

  • Prangishvili D, Forterre P, Garrett RA (2006) Viruses of the archaea: a unifying view. Nat Rev Micro 4:837–848

    Article  CAS  Google Scholar 

  • Quatrini R, Veloso F, Jedlicki E, Holmes DS (2004) Bioinformatic analysis of iron uptake in Acidithiobacillus ferrooxidans. In: Tsezos M, Hatzikioseyian A, Remoudaki E (eds) BioHydrometallurgy: a sustainable technology in evolution. National Technical University of Athens, Athens, pp 989–996

    Google Scholar 

  • Quatrini R, Jedlicki E, Holmes DS (2005a) Genomic insights into the iron uptake mechanisms of the biomining microorganism Acidithiobacillus ferrooxidans. J Ind Microbiol Biotechnol 32:606–614

    Article  CAS  Google Scholar 

  • Quatrini R, Lefimil C, Holmes DS, Jedlicki E (2005b) The ferric iron uptake regulator (Fur) from the extreme acidophile Acidithiobacillus ferrooxidans. Microbiology 151:2005–2015

    Article  CAS  Google Scholar 

  • Quatrini R, Lefimil C, Veloso F, Pedroso I (2007a) Bioinformatic prediction and experimental verification of Fur-regulated genes in the extreme acidophile Acidithiobacillus ferrooxidans. Nucleic Acids Res 35:2153–2166

    Article  CAS  Google Scholar 

  • Quatrini R, Martinez V, Osorio H, Veloso F, Pedroso I, Valdes J, Jedlicki E, Holmes DS (2007b) Iron homeostasis strategies in acidophilic iron oxidizers: comparative genome analysis. Adv Mater Res 20–21:439–442

    Google Scholar 

  • Quatrini R, Valdes J, Jedlicki E, Holmes D (2007c) The use of bioinformatics and genome biology to advance our understanding of bioleaching microorganisms. In: Donati E, Sand W (eds) Microbial processing of metal sulfides. Springer, Netherlands, pp 221–239

    Chapter  Google Scholar 

  • Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC II, Shah M, Hettich RL, Banfield JF (2005) Community proteomics of a natural microbial biofilm. Science 308:1915–1920

    Article  CAS  Google Scholar 

  • Rawlings DE (2005) The evolution of pTF-FC2 and pTC-F14, two related plasmids of the IncQ-family. Plasmid 53:137–147

    Article  CAS  Google Scholar 

  • Rawlings DE, Johnson DB (2007) The microbiology of biomining: development and optimization of mineral-oxidizing microbial consortia. Microbiology 153:315–324

    Article  CAS  Google Scholar 

  • Rawlings DE, Kusano T (1994) Molecular genetics of Thiobacillus ferrooxidans. Microbiol Mol Biol Rev 58:39–55

    CAS  Google Scholar 

  • Redder P, Garrett RA (2006) Mutations and rearrangements in the genome of Sulfolobus solfataricus P2. J Bacteriol 188:4198–4206

    Article  CAS  Google Scholar 

  • Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ (2009) Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci 106:8605–8610

    Article  CAS  Google Scholar 

  • Reysenbach A-L, Hamamura N, Podar M, Griffiths E, Ferreira S, Hochstein R, Heidelberg J, Johnson J, Mead D, Pohorille A, Sarmiento M, Schweighofer K, Seshadri R, Voytek MA (2009) Complete and draft genome sequences of six members of the aquificales. J Bacteriol 191:1992–1993

    Article  CAS  Google Scholar 

  • Rivas M, Seeger M, Holmes DS, Jedlicki E (2005) A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus ferrooxidans. Biological Res 38:283–297

    CAS  Google Scholar 

  • Rivas M, Seeger M, Jedlicki E, Holmes DS (2007) Second acyl homoserine lactone production system in the extreme acidophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 73:3225–3231

    Article  CAS  Google Scholar 

  • Ruepp A, Graml W, Santos-Martinez M-L, Koretke KK, Volker C, Mewes HW, Frishman D, Stocker S, Lupas AN, Baumeister W (2000) The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407:508–513

    Article  CAS  Google Scholar 

  • Schippers A, Breuker A, Blazejak A, Bosecker K, Kock D, Wright TL (2010) The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy (in press)

  • Selkov E, Overbeek R, Kogan Y, Chu L, Vonstein V, Holmes D, Silver S, Haselkorn R, Fonstein M (2000) Functional analysis of gapped microbial genomes: amino acid metabolism of Thiobacillus ferrooxidans. Proc Natl Acad Sci USA 97:3509–3514

    Article  CAS  Google Scholar 

  • She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC-Y, Clausen IG, Curtis BA, De Moors A, Erauso G, Fletcher C, Gordon PMK, Heikamp-de Jong I, Jeffries AC, Kozera CJ, Medina N, Peng X, Thi-Ngoc HP, Redder P, Schenk ME, Theriault C, Tolstrup N, Charlebois RL, Doolittle WF, Duguet M, Gaasterland T, Garrett RA, Ragan MA, Sensen CW, Van der Oost J (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci USA 98:7835–7840

    Article  CAS  Google Scholar 

  • Shmaryahu A, Holmes DS (2007) Discovery of small regulatory RNAs in the extremophile acidithiobacillus genus suggests novel genetic regulation. Adv Mater Res 20–21:535–538

    Article  Google Scholar 

  • Shmaryahu A, Lefimil C, Jedlicki E, Holmes DS (2009) Small regulatory RNA genes in Acidithiobacillus ferrooxidans: case studies of 6 S RNA and frr. Adv Mater Res 71–73:191–194

    Article  Google Scholar 

  • Siezen RJ, Wilson G (2009) Bioleaching genomics. Microb Biotechnol 2:297–303

    Article  CAS  Google Scholar 

  • Simmons SL, DiBartolo G, Denef VJ, Goltsman DSA, Thelen MP, Banfield JF (2008) Population genomic analysis of strain variation in leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol 6:e177

    Article  CAS  Google Scholar 

  • Soulère L, Guiliani N, Queneau Y, Jerez C, Doutheau A (2008) Molecular insights into quorum sensing in Acidithiobacillus ferrooxidans bacteria via molecular modelling of the transcriptional regulator AfeR and of the binding mode of long-chain acyl homoserine lactones. J Mol Model 14:599–606

    Article  CAS  Google Scholar 

  • Tuffin IM, de Groot P, Deane SM, Rawlings DE (2005) An unusual Tn21-like transposon containing an ars operon is present in highly arsenic-resistant strains of the biomining bacterium Acidithiobacillus caldus. Microbiology 151:3027–3039

    Article  CAS  Google Scholar 

  • Tuffin IM, Hector SB, Deane SM, Rawlings DE (2006) Resistance determinants of a highly arsenic-resistant strain of Leptospirillum ferriphilum isolated from a commercial biooxidation tank. Appl Environ Microbiol 72:2247–2253

    Article  CAS  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43

    Article  CAS  Google Scholar 

  • Valdés JH, Holmes DS (2009) Genomic lessons from biomining organisms: case study of the acidithiobacillus genus. Adv Mater Res 71–73:215–218

    Article  Google Scholar 

  • Valdés J, Veloso F, Jedlicki E, Holmes D (2003) Metabolic reconstruction of sulfur assimilation in the extremophile Acidithiobacillus ferrooxidans based on genome analysis. BMC Genomics 4:51

    Article  Google Scholar 

  • Valdés J, Pedroso I, Quatrini R, Dodson R, Tettelin H, Blake R, Eisen J, Holmes D (2008a) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597

    Article  CAS  Google Scholar 

  • Valdés J, Pedroso I, Quatrini R, Holmes DS (2008b) Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: insights into their metabolism and ecophysiology. Hydrometallurgy 94:180–184

    Article  CAS  Google Scholar 

  • Valdés J, Quatrini R, Hallberg K, Mangold S, Dopson M, Valenzuela PTD, Holmes DS (2009) Draft genome sequence of the extremely acidophilic bacterium Acidithiobacillus caldus ATCC 51756 reveals metabolic versatility in the genus Acidithiobacillus. J Bacteriol 191:5877–5878

    Article  CAS  Google Scholar 

  • Valdés J, Osorio H, Lefimil C, Duarte F, Jedlicki E, Quatrini R, Holmes DS (2010) Comparative genomics begins to unravel the ecophysiology of bioleaching. Hydrometallurgy (in press)

  • Valenzuela L, Chi A, Beard S, Orell A, Guiliani N, Shabanowitz J, Hunt DF, Jerez CA (2006) Genomics, metagenomics and proteomics in biomining microorganisms. Biotechnol Adv 24:197–211

    Article  CAS  Google Scholar 

  • van Zyl LJ, Deane SM, Louw L-A, Rawlings DE (2008) Presence of a family of plasmids (29 to 65 Kilobases) with a 26-Kilobase common region in different strains of the sulfur-oxidizing bacterium Acidithiobacillus caldus. Appl Environ Microbiol 74:4300–4308

    Article  CAS  Google Scholar 

  • VerBerkmoes NC, Denef VJ, Hettich RL, Banfield JF (2009) Systems biology: functional analysis of natural microbial consortia using community proteomics. Nat Rev Micro 7:196–205

    Article  CAS  Google Scholar 

  • Wächtershäuser G (1988) Before enzymes and templates: theory of surface metabolism. Microbiol Rev 52:452–484

    Google Scholar 

  • Wächtershäuser G (2007) On the chemistry and evolution of the pioneer organism. Chem Biodivers 4:584–602

    Article  Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  CAS  Google Scholar 

  • Whitaker RJ, Banfield JF (2006) Population genomics in natural microbial communities. Trends Ecol Evol 21:508–516

    Article  Google Scholar 

  • Wood AP, Aurikko JP, Kelly DP (2004) A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy? FEMS Microbiol Rev 28:335–352

    Article  CAS  Google Scholar 

  • Yamada T, Hiraoka Y, Das Gupta TK, Chakrabarty AM (2004) Rusticyanin, a bacterial electron transfer protein, causes G1 arrest in J774 and apoptosis in human cancer cells. Cell Cycle 3:1182–1187

    CAS  Google Scholar 

  • Yates JR, Holmes DS (1987) Two families of repeated DNA sequences in Thiobacillus ferrooxidans. J Bacteriol 169:1861–1870

    CAS  Google Scholar 

  • Zhao HL, Holmes DS (1993) Insertion sequence IST1 and associated phenotypic switching in Thiobacillus ferrooxidans. In: A. E. Torma, M. L. Apel, and C. L. Brierley (eds) Biohydrometallurgical technologies, TMS Press, Warrendale, PA, 2:667–671

Download references

Acknowledgments

The authors thank Fondecyt 1090451 and 1100887, UNAB DI-15-06-I, Conicyt Basal CCTE PFB16, Innova 08CM01-03, and Conicyt postgraduate studies grant 2010.

Author information

Author notes

  1. Jorge Valdés

    Present address: Computational Genomics Laboratory, Center for Bioinformatics and Molecular Simulations, Universidad de Talca, Santiago, Chile

Authors and Affiliations

  1. Center for Bioinformatics and Genome Biology, Fundación Ciencia para la Vida, Avda. Zanartu 1482, Santiago, Chile

    Juan Pablo Cárdenas, Jorge Valdés, Raquel Quatrini, Francisco Duarte & David S. Holmes

  2. Depto. de Ciencias Biológicas, Facultad de Ciencias Biológicas, Universidad Andrés Bello, Santiago, Chile

    Juan Pablo Cárdenas, Jorge Valdés, Francisco Duarte & David S. Holmes

Authors
  1. Juan Pablo Cárdenas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Valdés
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raquel Quatrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David S. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David S. Holmes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cárdenas, J.P., Valdés, J., Quatrini, R. et al. Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms. Appl Microbiol Biotechnol 88, 605–620 (2010). https://doi.org/10.1007/s00253-010-2795-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-010-2795-9

Keywords

Search

Navigation