Skip to main content

The Dynamic Genomes of Acidophiles

  • Chapter
  • First Online:
Polyextremophiles

Abstract

The large-scale sequencing of microbial genomes and environmental samples in the last decade has revealed a huge amount of genetic diversity in natural populations. Extremophilic species in which the genomes of independently isolated strains have been sequenced often show a high variance in gene content as well as the pervasive effects of genomic rearrangements due to recombination. On the other hand, metagenomic studies have highlighted the dynamic complexity of bacterial populations and the action of mobile elements (plasmids, phage, and transposons) in shaping the genetic makeup of these organisms. Here we review the lessons gained from studies of the genomes, transcriptomes, and proteomes of acidophilic bacteria, with emphasis on what is known about the mechanisms that generate diversity and favor genetic exchange in acidic environments. Genome plasticity due to the combination of horizontal gene transfer (HGT) and the activity of mobile genetic elements (mobilome) could be essential during ecological specialization and adaptation to extreme environments.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Angelov A, Liebl W (2006) Insights into extreme thermoacidophily based on genome analysis of Picrophilus torridus and other thermoacidophilic archaea. J Biotechnol 126:3–10

    Article  PubMed  CAS  Google Scholar 

  • Arsene-Ploetze F, Koechler S, Marchal M, Coppee JY, 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, Lievremont 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, Medigue C, Bertin PN (2010) Structure, function, and evolution of the Thiomonas spp. genome. PLoS Genet 6:e1000859

    Article  PubMed  Google Scholar 

  • Aucelli T, Contursi P, Girfoglio M, Rossi M, Cannio R (2006) A spreadable, non-integrative and high copy number shuttle vector for Sulfolobus solfataricus based on the genetic element pSSVx from Sulfolobus islandicus. Nucleic Acids Res 34:e114

    Article  PubMed  Google Scholar 

  • Auernik KS, Cooper CR, Kelly RM (2008) Life in hot acid: pathway analyses in extremely thermoacidophilic archaea. Curr Opin Biotechnol 19:445–453

    Article  PubMed  CAS  Google Scholar 

  • Aziz RK, Breitbart M, Edwards RA (2010) Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 38:4207–4217

    Article  PubMed  CAS  Google Scholar 

  • Banfield JF, Young M (2009) Microbiology. Variety – the splice of life – in microbial communities. Science 326:1198–1199

    Article  PubMed  CAS  Google Scholar 

  • Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    Article  PubMed  CAS  Google Scholar 

  • Boyd EF, Almagro-Moreno S, Parent MA (2009) Genomic islands are dynamic, ancient integrative elements in bacterial evolution. Trends Microbiol 17:47–53

    Article  PubMed  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  PubMed  Google Scholar 

  • Cadillo-Quiroz H, Didelot X, Held NL, Herrera A, Darling A, Reno ML, Krause DJ, Whitaker RJ (2012) Patterns of gene flow define species of thermophilic Archaea. PLoS Biol 10:e1001265

    Article  PubMed  CAS  Google Scholar 

  • Cardénas JP, Valdes J, Quatrini R, Duarte F, Holmes DS (2010) Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms. Appl Microbiol Biotechnol 88:605–620

    Article  PubMed  Google Scholar 

  • Coleman ML, Sullivan MB, Martiny AC, Steglich C, Barry K, DeLong EF, Chisholm SW (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311:1768–1770

    Article  PubMed  CAS  Google Scholar 

  • Denef VJ, Banfield JF (2012) In situ evolutionary rate measurements show ecological success of recently emerged bacterial hybrids. Science 336:462–466

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Eppley JM, Tyson GW, Getz WM, Banfield JF (2007) Genetic exchange across a species boundary in the archaeal genus Ferroplasma. Genetics 177:407–416

    Article  PubMed  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 U S A 101:9091–9096

    Article  PubMed  Google Scholar 

  • Garrett RA, Shah SA, Vestergaard G, Deng L, Gudbergsdottir S, Kenchappa CS, Erdmann S, She Q (2011) CRISPR-based immune systems of the Sulfolobales: complexity and diversity. Biochem Soc Trans 39:51–57

    Article  PubMed  CAS  Google Scholar 

  • Glenn AW, Roberto FF, Ward TE (1992) Transformation of Acidiphilium by electroporation and conjugation. Can J Microbiol 38:387–393

    Article  PubMed  CAS  Google Scholar 

  • Goltsman DS, 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  PubMed  CAS  Google Scholar 

  • Grogan DW, Ozarzak MA, Bernander R (2008) Variation in gene content among geographically diverse Sulfolobus isolates. Environ Microbiol 10:137–146

    PubMed  CAS  Google Scholar 

  • Held NL, Herrera A, Cadillo-Quiroz H, Whitaker RJ (2010) CRISPR associated diversity within a population of Sulfolobus islandicus. PLoS One 5:e12988

    Article  PubMed  Google Scholar 

  • Hess M (2008) Thermoacidophilic proteins for biofuel production. Trends Microbiol 16:414–419

    Article  PubMed  CAS  Google Scholar 

  • Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393

    Article  PubMed  CAS  Google Scholar 

  • Kondrat’eva TF, Danilevich VN, Ageeva SN, Karavaiko GI (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  PubMed  Google Scholar 

  • Lang AS, Zhaxybayeva O, Beatty JT (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol 10:472–482

    PubMed  CAS  Google Scholar 

  • Leigh JA, Albers SV, Atomi H, Allers T (2011) Model organisms for genetics in the domain Archaea: methanogens, halophiles, Thermococcales and Sulfolobales. FEMS Microbiol Rev 35:577–608

    Article  PubMed  CAS  Google Scholar 

  • Lintner NG, Frankel KA, Tsutakawa SE, Alsbury DL, Copie V, Young MJ, Tainer JA, Lawrence CM (2011) The structure of the CRISPR-associated protein Csa3 provides insight into the regulation of the CRISPR/Cas system. J Mol Biol 405:939–955

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Maezato Y, Dana K, Blum P (2011) Engineering thermoacidophilic archaea using linear DNA recombination. Methods Mol Biol 765:435–445

    Article  PubMed  CAS  Google Scholar 

  • Martusewitsch E, Sensen CW, Schleper C (2000) High spontaneous mutation rate in the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by transposable elements. J Bacteriol 182:2574–2581

    Article  PubMed  CAS  Google Scholar 

  • Mi S, Song J, Lin J, Che Y, Zheng H, Lin J (2011) Complete genome of Leptospirillum ferriphilum ML-04 provides insight into its physiology and environmental adaptation. J Microbiol 49:890–901

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14:627–633

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Paz M, Gomez MJ, Arcas A, Parro V (2010) Environmental transcriptome analysis reveals physiological differences between biofilm and planktonic modes of life of the iron oxidizing bacteria Leptospirillum spp. in their natural microbial community. BMC Genomics 11:404

    Article  PubMed  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 6:374

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pina M, Bize A, Forterre P, Prangishvili D (2011) The archeoviruses. FEMS Microbiol Rev 35:1035–1054

    Article  PubMed  CAS  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  PubMed  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  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 U S A 106:8605–8610

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pašić L, Thingstad TF, Rohwer F, Mira A (2009) Explaining microbial population genomics through phage predation. Nat Rev Microbiol 7:828–836

    Article  PubMed  Google Scholar 

  • Siguier P, Filee J, Chandler M (2006a) Insertion sequences in prokaryotic genomes. Curr Opin Microbiol 9:526–531

    Article  PubMed  CAS  Google Scholar 

  • Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006b) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32–D36

    Article  PubMed  CAS  Google Scholar 

  • Simmons SL, Dibartolo G, Denef VJ, Goltsman DS, 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  PubMed  Google Scholar 

  • Snyder JC, Young MJ (2011) Advances in understanding archaea-virus interactions in controlled and natural environments. Curr Opin Microbiol 14:497–503

    Article  PubMed  Google Scholar 

  • Snyder JC, Wiedenheft B, Lavin M, Roberto FF, Spuhler J, Ortmann AC, Douglas T, Young M (2007) Virus movement maintains local virus population diversity. Proc Natl Acad Sci U S A 104:19102–19107

    Article  PubMed  Google Scholar 

  • Touchon M, Rocha EP (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24:969–981

    Article  PubMed  CAS  Google Scholar 

  • Toussaint A, Chandler M (2012) Prokaryote genome fluidity: toward a system approach of the mobilome. Methods Mol Biol 804:57–80

    Article  PubMed  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  PubMed  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  PubMed  CAS  Google Scholar 

  • Twiss E, Coros AM, Tavakoli NP, Derbyshire KM (2005) Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol Microbiol 57:1593–1607

    Article  PubMed  CAS  Google Scholar 

  • Tyson GW, Banfield JF (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10:200–207

    PubMed  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Valdés J, Cárdenas JP, Quatrini R, Esparza M, Osorio H, Duarte F, Lefimil C, Sepulveda R, Jedlicki E, Holmes DS (2010) Comparative genomics begins to unravel the ecophysiology of bioleaching. Hydrometallurgy 104:471–476

    Article  Google Scholar 

  • van Zyl LJ, Deane SM, Louw LA, 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  PubMed  Google Scholar 

  • Wagner A (2009) Transposable elements as genomic diseases. Mol Biosyst 5:32–35

    Article  PubMed  CAS  Google Scholar 

  • Wagner M, Berkner S, Ajon M, Driessen AJ, Lipps G, Albers SV (2009) Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus. Biochem Soc Trans 37:97–101

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Liu X, Liu S, Yu Y, Lin J, Lin J, Pang X, Zhao J (2012) Development of a markerless gene replacement system for Acidithiobacillus ferrooxidans and construction of a pfkB mutant. Appl Environ Microbiol 78:1826–1835

    Article  PubMed  CAS  Google Scholar 

  • Whitaker RJ, Grogan DW, Taylor JW (2005) Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol Biol Evol 22:2354–2361

    Article  PubMed  CAS  Google Scholar 

  • Wiedenheft B, Sternberg SH, Doudna JA (2010) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338

    Article  Google Scholar 

  • Wilmes P, Simmons SL, Denef VJ, Banfield JF (2009) The dynamic genetic repertoire of microbial communities. FEMS Microbiol Rev 33:109–132

    Article  PubMed  CAS  Google Scholar 

  • Xiang X, Chen L, Huang X, Luo Y, She Q, Huang L (2005) Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features. J Virol 79:8677–8686

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Funding for this work was provided by grants ERC-250350/IPBSL (FJLS, VPG), CGL2010-17384 (FJLdS, MJG), AYA2011-24803 (VPG) and Consolider INGENIO CSD2007-0005 (MJG). EGT was a recipient of an INTA training fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francisco J. López de Saro .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

de Saro, F.J.L., Gómez, M.J., González-Tortuero, E., Parro, V. (2013). The Dynamic Genomes of Acidophiles. In: Seckbach, J., Oren, A., Stan-Lotter, H. (eds) Polyextremophiles. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 27. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6488-0_3

Download citation

Publish with us

Policies and ethics