Skip to main content
SpringerLink
Log in

Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications

  • Review
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Acidophiles are ecologically and economically important group of microorganisms, which thrive in acidic natural (solfataric fields, sulfuric pools) as well as artificial man-made (areas associated with human activities such as mining of coal and metal ores) environments. They possess networked cellular adaptations to regulate pH inside the cell. Several extracellular enzymes from acidophiles are known to be functional at much lower pH than the cytoplasmic pH. Enzymes like amylases, proteases, ligases, cellulases, xylanases, α-glucosidases, endoglucanases, and esterases stable at low pH are known from various acidophilic microbes. The possibility of improving them by genetic engineering and directed evolution will further boost their industrial applications. Besides biocatalysts, other biomolecules such as plasmids, rusticynin, and maltose-binding protein have also been reported from acidophiles. Some strategies for circumventing the problems encountered in expressing genes encoding proteins from extreme acidophiles have been suggested. The investigations on the analysis of crystal structures of some acidophilic proteins have thrown light on their acid stability. Attempts are being made to use thermoacidophilic microbes for biofuel production from lignocellulosic biomass. The enzymes from acidophiles are mainly used in polymer degradation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Albers SV, Driessen AJ (2007) Conditions for gene disruption by homologous recombination of exogenous DNA into the Sulfolobus solfataricus genome. Archaea 2:145–149

    Article  Google Scholar 

  • Alikhajeh J, Khajeh K, Naderi-Manesh M, Ranjbar B, Sajedi RH, Naderi-Manesh H (2007) Kinetic analysis, structural studies and prediction of pKa values of Bacillus KR-8104 α-amylase: the determinants of pH-activity profile. Enzym Microbiol Technol 41:337–345

    Article  CAS  Google Scholar 

  • Arpigny JL, Jaeger K-E (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343:177–183

    Article  PubMed  CAS  Google Scholar 

  • Asghari SM, Khajeh K, Moradian F, Ranjbar B, Naderi-Manesh H (2004) Acid-induced conformational changes in Bacillus amyloliqefaciens α-amylase: appearance of a molten globule like state. Enzym Microb Technol 35:51–57

    Article  CAS  Google Scholar 

  • Asoodeh A, Chamani J, Lagzian M (2010) A novel thermostable, acidophilic α-amylase from a new thermophilic “Bacillus sp. Ferdowsicous” isolated from Ferdows hot mineral spring in Iran: purification and biochemical characterization. Int J Biol Macromol 46:289–297

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Auernik KS, Maezato Y, Blum PH, Kelly RM (2008b) 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  PubMed  CAS  Google Scholar 

  • Baker-Austin C, Dopson M (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15:165–171

    Article  PubMed  CAS  Google Scholar 

  • Batrakov SG, Pivovarova TA, Esipov SE, Sheichenko VI, Karavaiko GI (2002) Beta-d-glycopyranosyl caldarchaetidylglycerol is the main lipid of the acidophilic, mesophilic, ferrous iron-oxidizing archaeon Ferroplasm acidiphilum. Biochim Biophys Acta Mol Cell Biol Lipids 1581:29–35

    CAS  Google Scholar 

  • Bertoldo C, Dock C, Antranikian G (2004) Thermoacidophilic microorganisms and their novel biocatalysts. Eng Life Sci 4:521–531

    Article  CAS  Google Scholar 

  • Bhattacharyya S, Chakrabarty BK, Das A, Jundu P, Banerjee PC (1990) Acidiphilium symbioticum sp. nov., an acidophilic heterotrophic bacterium from Thiobacillus ferrooxidans cultures isolated from Indian mines. Can J Microbiol 37:78–85

    Article  Google Scholar 

  • Biely P (1985) Microbial xylanolytic systems. Trends Biotechnol 11:286–290

    Article  Google Scholar 

  • Blake RC, White KJ, Shute EA (1991) Effect of divers anions on the electron-transfer reaction between iron and rusticyanin from Thiobacillus ferrooxidans. Biochemistry 30:9443–9449

    Article  PubMed  CAS  Google Scholar 

  • Blanco A, Diaz P, Martinez J, Vidal T, Torres AL, Pastor FI (1998) Cloning of a new endoglucanase gene from Bacillus sp. BP-23 and characterization of the enzyme performance in paper manufacture from cereal straw. Appl Microbiol Biotechnol 50:48–54

    Article  PubMed  CAS  Google Scholar 

  • Brierley CL, Brierley JA (1973) A chemoautotropic and thermophilic microorganism isolated from an acid hot spring. Can J Microbiol 19:183–188

    Article  PubMed  CAS  Google Scholar 

  • Brock TD, Brock KM, Belly RT, Weiss RL (1972) Sulfolobus: a new genus of sulphur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 84:54–68

    Article  PubMed  CAS  Google Scholar 

  • Bryant RD, McGoarty KM, Costerton JW, Laishley EJ (1983) Isolation and characterisation of a new acidophilic Thiobacillus strain (T. albertis). Can J Microbiol 29:1159–1170

    Google Scholar 

  • Buonocore V, Caporale C, Derosa M, Gambacorta A (1976) Stable, inducible, thermoacidophilic α-amylase from Bacillus acidocaldarius. J Bacteriol 128:515–521

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790

    Article  CAS  Google Scholar 

  • Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23

    Article  PubMed  CAS  Google Scholar 

  • Crabb WD, Shetty JK (1999) Commodity scale production of sugars from starches. Curr Opin Microbiol 2:252–256

    Article  PubMed  CAS  Google Scholar 

  • Crossman L, Holden M, Pain A, Parkhill J (2004) Genomes beyond compare. Nat Rev Microbiol 2:616–617

    Article  PubMed  CAS  Google Scholar 

  • Darland G, Brock TD (1971) Bacillus acidocaldarius sp. nov., an acidophilic, thermophilic spore forming bacterium. J Gen Microbiol 67:9–15

    Google Scholar 

  • Darland G, Brock TD, Samsonoff W, Conti SF (1970) A thermophilic, acidophilic mycoplasma isolated from a coal refuse pile. Science 170:1416–1418

    Article  PubMed  CAS  Google Scholar 

  • Davies DR (1990) The structure and function of the aspartic proteinases. Ann Rev Biophys Chem 19:189–215

    Article  CAS  Google Scholar 

  • De Pascale D, Sasso MP, Lernia ID, Lazzaro AD, Furia A, Farina MC, Rossi M, De rosa M (2001) Recombinant thermophilic enzymes from trehalose and trehalosyl dextrins production. J Mol Catal B Enzym 11:777–786

    Article  Google Scholar 

  • Di Lernia I, Morana A, Ottombrino A, Fusco S, Rossi M, De Rosa M (1998) Enzymes from Sulfolobus shibatae for the production of trehalose and glucose from starch. Extremophiles 2:409–416

    Article  PubMed  CAS  Google Scholar 

  • Dock C, Hess M, Anthranikian G (2008) A thermoactive glucoamylase with biotechnological relevance from the thermoacidophilic euryarchaeon Thermoplasma acidophilum. Appl Microbiol Biotechnol 78:105–114

    Article  PubMed  CAS  Google Scholar 

  • Eckert K, Schneider E (2003) A thermoacidophilic endoglucanase (CelB) from Alicyclobacillus acidocaldarius displays high sequence similarity to arabinofuranosidases belonging to family 51 of glycoside hydrolases. Eur J Biochem 270:3593–3602

    Article  PubMed  CAS  Google Scholar 

  • Ettema TJ, Brinkman AB, Lamers PP, Kornet NG, de Vos WM, Vander Oost J (2006) Molecular characterization of a conserved archaeal copper resistance (cop) gene cluster and its copper responsive regulator in Sulfolobus solfataricus P2. Microbiology 152:1969–1979

    Article  PubMed  CAS  Google Scholar 

  • Fang T-Y, Huang X-G, Shih T-Y, Tseng W-C (2004) Characterization of trehalosyl dextrin forming enzyme from thermophilic archaeon Sulfolobus solfataricus ATCC 35092. Extremophiles 8:335–343

    Article  PubMed  CAS  Google Scholar 

  • Ferrer M, Golyshina OV, Beloqui A, Bottger LH, Andreu JM, Polaina J, Lacey ALD, Trautwein AX, Timmis KN, Golyshin PN (2008) A purple acidophilic di-ferric DNA ligase from Ferroplasma. Proc Natl Acad Sci USA 105:8878–8883

    Article  PubMed  CAS  Google Scholar 

  • Fuchs T, Huber H, Teiner K, Burggraf S, Stetter KO (1996) Metallosphaera prunae, sp. nov., a novel metal-mobilizing, thermoacidophilic archaeum, isolated from a uranium mine in Germany. Syst Appl Microbiol 18:560–566

    Google Scholar 

  • Fusek M, Lin XL, Tang J (1990) Enzymatic properties of thermopsin. J Biol Chem 265:1496–1501

    PubMed  CAS  Google Scholar 

  • Futterer 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  PubMed  CAS  Google Scholar 

  • Gaffney PJ, Edgell TA, Dawson PA, Ford AW, Stocker E (1996) A pig collagen peptide fraction. A unique material for maintaining biological activity during lyophilization and during storage in the liquid state. J Pharm Pharmacol 48:896–898

    Article  PubMed  CAS  Google Scholar 

  • Galbe M, Zacchi G (2007) Pretreatment of lignocellulosic materials for efficient bioethanol production. Adv Biochem Eng Biotechnol 108:41–65

    PubMed  CAS  Google Scholar 

  • Golovacheva RS, Golyshina OV, Karavaiko GI, Dorofeev AG, Cheruykh NA (1992) The new iron-oxidizing bacterium Leptospirillum thermoferrooxidans sp. nov. Mikrobiologiya 61:1056–1065

  • Golovacheva RS, Karavaiko GI (1978) A new genus of thermophilic spore-forming bacteria, Sulfobacillus. Mikrobiologiya 47:815–822

    CAS  Google Scholar 

  • Golyshina OV, Golyshina NP, Timmis NK, Ferrer M (2006) The pH optimum anomaly of intracellular enzymes of Ferroplasma acidiphilum. Environ Microbiol 8:416–425

    Article  PubMed  CAS  Google Scholar 

  • Golyshina OV, Pivovarova TA, Karavaiko GI, Moore ERB, Abracham WR, Luensdorf H, Timmis KN, Yakimov MM, Golyshin PN (2000) Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic autotrophic, ferrous-iron oxidizing, cell wall lacking, mesophilic member of the Ferroplasmaceae fam. Nov., comprising distinct lineage of Archaea. Int J Syst Evol Microbiol 50:997–1006

    Article  PubMed  CAS  Google Scholar 

  • Grogan D, Palm P, Zillig W (1990) Isolate B12 which harbors a virus-like element represents a new species of the archaebacterial genus Sulfolobus, Sulfolobus shibatae new species. Arch Mikrobiol 154:594–599

    CAS  Google Scholar 

  • Guay R, Silver M (1975) Thiobacillus acidophilus sp. nov., isolation and some physiological characteristics. Can J Microbiol 21:281–288

    Article  PubMed  CAS  Google Scholar 

  • Gueguen Y, Rolland JL, Schroeck S, Flament D, Defretin S, Saniez MH, Dietrich J (2001) Characterization of the maltooligosyl trehalose synthese from the thermophilic archaeon Sulfolobus acidocaldarius. FEMS Microbiol Lett 194:201–206

    Article  PubMed  CAS  Google Scholar 

  • Han D, Krauss G (2009) Characterization of the endonuclease SSO2001 from Sulfolobus solfataricus P2. FEBS Lett 583:771–776

    Article  PubMed  CAS  Google Scholar 

  • Harrison AP (1981) Acidiphilium cryptum gen. nov., sp. nov., heterotrophic bacterium from acidic mineral environments. Int J Syst Bacteriol 31:327–332

    Article  Google Scholar 

  • Harrison AP (1983) Genomic and physiological comparisons between heterotrophic thiobacilli and Acidiphilium cryptum, Thiobacillus versutus, sp. nov., and Thiobacillus acidophilus nom. rev. Int J Syst Bacteriol 33:211–217

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hirata A, Adachi M, Sekine A, Kang YN, Utsumi S, Mikami B (2004) Structural and enzymatic analysis of soybean beta-amylase mutants with increased pH optimum. J Biol Chem 279:7287–7295

    Article  PubMed  CAS  Google Scholar 

  • Honda S (1998) Dietary use of collagen and collagen peptides for cosmetics. Food Style 21:54–60

    Google Scholar 

  • Hou S, Makarova KS, Saw JHW, Senin P, Ly BV, Zhou Z, RenY Wang J, Galperin MY, Omelchenko MV, Wolf YI, Yutin N, Koonin EV, Stott MB, Mountain BW, Crowe MA, Smirnova AV, Dunfield PF, 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  PubMed  CAS  Google Scholar 

  • Hovarth P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170

    Article  CAS  Google Scholar 

  • Huang Y, Krauss G, Cottaz S, Driguez H, Lipps G (2005) A highly acid-stable and thermostable endo-b-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochem J 385:581–588

    Article  PubMed  CAS  Google Scholar 

  • Huber G, Spinnler C, Gambacorta A, Stetter KO (1989) Metallosphaera sedula gen. and sp. nov. represents a new genus of aerobic, metal-mobilizing, thermoacido-philic archaebacteria. Syst Appl Microbiol 12:38–47

    Google Scholar 

  • Huber H, Stetter KO (1989) Thiobacillus prosperus sp. nov., represents of new group of acid tolerant metal-mobilizing bacteria isolated from a marine geothermal field. Arch Mikrobiol 151:479–485

    CAS  Google Scholar 

  • Huber G, Stetter KO (1991) Sulfolobus metallicus, sp. nov., a novel strictly chemolithoautotrophic thermophilic archaeal species of metal mobilizers. Syst Appl Microbiol 14:372–378

    CAS  Google Scholar 

  • Inagaki K, Nakahira K, Mukai K, Tamura T, Tanaka H (1998) Gene cloning and characterization of an acidic xylanase from Acidobacterium capsulatum. Biosci Biotechnol Biochem 62:1061–1067

    Article  PubMed  CAS  Google Scholar 

  • Itoh T, Yoshikawa N, Takashina T (2007) Thermogymnomonas acidicola gen. nov., sp. nov., a novel thermoacidophilic, cell wall-less archaeon in the order Thermoplasmatales, isolated from a solfataric soil in Hakone, Japan. Int J Syst Evol Microbiol 57:2557–2561

    Article  PubMed  CAS  Google Scholar 

  • Jones A, Lamsa M, Frandsen TP, Spendler T, Harris P, Sloma A, Xu F, Nielson JB, Cherry JR (2008) Directed evolution of a maltogenic alpha-amylase from Bacillus sp. TS-25. J Biotechnol 134:325–333

    Article  PubMed  CAS  Google Scholar 

  • Karavaiko GI, Golyshina OV, Troitskii AV, Valiehoroman KM, Golovacheva RS, Pivovarova TA (1994) Sulfurococcus yellowstonii sp. nov., a new species of ironoxidizing and sulphur-oxidizing thermoacidophilic archaebacteria. Mikrobiologiya 63:379–387

    Google Scholar 

  • Katkocin DM (1985) Thermostable glucoamylase and method for its production. US Patent No. 4,536,477

  • Kato M (1999) Trehalose production with a new enzymatic system from Sulfolobus solfataricus KM1. J Mol Catal B Enzym 6:223–233

    Article  CAS  Google Scholar 

  • Kato M, Miura Y, Kettoku M, Komeda T, Iwamatsu A, Kobayashi K (1996a) Reaction mechanism of a new glycosyltrehalose hydrolyzing enzyme isolated from the hyperthermophilic archaeon, Sulfolobus solfataricus KM1. Biosci Biotechnol Biochem 60:925–928

    Article  CAS  Google Scholar 

  • Kato M, Miura Y, Kettoku M, Shindo K, Iwamatsu A, Kobayashi K (1996b) Purification and characterization of new trehalose producing enzymes isolated from the hyperthermophilic archaean, Sulfolobus solfataricus KM1. Biosci Biotechnol Biochem 60:546–550

    Article  PubMed  CAS  Google Scholar 

  • Kawarabayasi Y, Hino Y, Horikawa H, Jin-no K, Takahashi M, Sekine M, Baba S, 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, Aoki K, 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  PubMed  CAS  Google Scholar 

  • Kawashima T, Amano N, Koike H, Makino S, Higuchi S, Kawashima-Ohya Y, Watanabe K, Yanazaki M, Kanehori K, Kawamotoi 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  PubMed  CAS  Google Scholar 

  • Keeling PJ, Klenk H-P, Singh RK, Feeley O, Schleper C, Zillig W, Doolittle WF, Sensen WC (1996) Complete nucleotide sequence of the Sulfolobus islandicus multicopy plasmid pRN1. Plasmid 35:141–144

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ, Klenk HP, Singh RK, Schenk ME, Sensen WC, Zillig W, Doolittle WF (1998) Sulfolobus islandicus plasmids pRN1 and pRN2 share distant but common evolutionary ancestry. Extremophiles 2:391–393

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Lee SB (2006) Rare codon clusters at 5′-end influence heterologous expression of archaeal gene in Escherichia coli. Protein Expr Purif 50:49–57

    Article  PubMed  CAS  Google Scholar 

  • Kim M, Park J, Kim Y, Lee H, Nyawira R, Shin H, Park C, Yoo S, Kim Y, Moon T, Park K (2004) Properties of novel thermostable glucoamylase from the hyperthermophilic archaeon Sulfolobus solfataricus in relation to starch processing. Appl Environ Microbiol 70:3933–3940

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto N, Inagaki K, Sugio T, Tano T (1991) Purification and properties of an acidic β-glucosidase from Acidobacterium capsulatum. J Fermen Bioeng 71:318–321

    Article  CAS  Google Scholar 

  • Kishimoto N, Kosako Y, Eakao N, Tano T, Hiraishi A (1995) Transfer of Acidiphilium facilis and Acidiphilium aminolytica to the genus Acidocella gen. nov., and emendation of the genus Acidiphilium. Syst Appl Microbiol 18:85–91

    Article  Google Scholar 

  • Kletzin A, Lieke A, Urich T, Charlebois RL, Sensen CW (1999) Molecular analysis of pDL10 from Acidianus ambivalens reveals a family of related plasmids from extremely thermophilic and acidophilic archaea. Genetics 152:1307–1314

    PubMed  CAS  Google Scholar 

  • Kocabayak S, Ozel H (2007) An extracellular Pepstatin insensitive acid protease produced by Thermoplasma volcanium. Biores Technol 98:112–117

    Article  CAS  Google Scholar 

  • Koma D, Sawai T, Harayama S, Kino K (2006) Overexpression of the genes from thermophiles in Escherichia coli at high-temperature cultivation. Appl Microbiol Biotechnol 73:172–180

    Article  PubMed  CAS  Google Scholar 

  • Kurosawa N, Itoh YH, Iwai T, Sugai A, Uda I, Kimura N, Horiuchi T, Itoh T (1998) Sulfurisphaera ohwakuensis gen. nov., sp. nov., a novel extremely thermophilic acidophile of the order Sulfolobales. Int J Syst Bacteriol 48:451–456

    Google Scholar 

  • Kurosawa N, Fukuda K, Itoh YH, Horiuchi T (2000) Partial purification and characterization of thermostable acid phosphatase from thermoacidophilic archaeon Sulfolobus acidocaldarius. Curr Microbiol 40:57–60

    Article  PubMed  CAS  Google Scholar 

  • Limauro DR, Cannio G, Fiorentino MR, Bartolucci S (2001) Identification and molecular characterization of an endoglucanase gene, CelS, from the extremely thermophilic archaeon Sulfolobus solfataricus. Extremophiles 5:213–219

    Article  PubMed  CAS  Google Scholar 

  • Liu XD, Xu Y (2008) A novel raw starch digesting α-amylase from a newly isolated Bacillus sp. YX-1: purification and characterization. Biores Technol 99:4315–4320

    Article  CAS  Google Scholar 

  • Lobos JH, Chisholm TE, Bopp LH, Holmes DS (1986) Acidiphilium organovorum sp. nov., an acidophilic heterotroph isolated from a Thiobacillus ferrooxidans culture. Int J Syst Bacteriol 36:139–144

    Article  CAS  Google Scholar 

  • Macalady JL, Vestling MM, Baumler D, Boekelheide N, Kaspar CW, Banfield JF (2004) Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid. Extremophiles 8:411–419

    Article  PubMed  CAS  Google Scholar 

  • Manabe F, Itoh YH, Shoun H, Wakagi T (2009) Membrane-bound acid pyrophosphatase from Sulfolobus tokodaii, a thermoacidophilic archaeon: heterologous expression of the gene and characterization of the product. Extremophiles 13:859–865

    Article  PubMed  CAS  Google Scholar 

  • Manabe F, Shoun H, Wakagi T (2011) Conserved residues in membrane-bound acid pyrophosphatase from Sulfolobus tokodaii, a thermoacidophilic archaeon. Extremophiles 15:359–364

    Article  PubMed  CAS  Google Scholar 

  • Marciniszyn J, Hartsuck JA, Tang J (1976) Mode of inhibition of acid proteases by pepstatin. J Biol Chem 251:7088–7094

    PubMed  CAS  Google Scholar 

  • Markosyan GE (1972) A new iron-oxidizing bacterium Leptospirillum ferrooxidans gen. nov., sp. nov. Biol J Armenia 25:26–29

    Google Scholar 

  • Markosyan GE (1973) A new mixotrophic sulphur bacterium developing in acid media, Thiobacillus organoparus sp. Dokl Akad Nauk SSSR 211:1205–1208

    Google Scholar 

  • Matin A (1999) pH homeostasis in acidophiles. Novartis Found Sym 221:152–163

    CAS  Google Scholar 

  • Matzke J, Herrmann A, Schneider E, Bakker EP (2000) Gene cloning, nucleotide sequence and biochemical properties of a cytoplasmic cyclomaltodextrinase (neopullulanase) from Alicyclobacillus acidocaldarius, reclassification of a group of enzymes. FEMS Microbiol Lett 183:55–61

    Article  PubMed  CAS  Google Scholar 

  • Matzke J, Schwermann B, Baker EP (1997) Acidostable and acidophilic proteins: the example of the α- amylase from Alicyclobacillus acidocaldarius. Comp Biochem Physiol 118A:475–479

    Article  CAS  Google Scholar 

  • Maurelli L, Giovane A, Esposito A, Moracci M, Fiume I, Rossi M, Morana A (2008) Evidence that the xylanase activity from Sulfolobus solfataricus Oα is encoded by the endoglucanase precursor gene (sso1354) and characterization of the associated cellulase activity. Extremophiles 12:689–700

    Article  PubMed  CAS  Google Scholar 

  • Miura Y, Kettoku M, Kato M, Kobayashi K, Kondo K (1999) High level production of thermostable alpha-amylase from Sulfolobus solfataricus in high-cell density culture of the food yeast Candida utilis. J Mol Microbiol Biotechnol 1:129–134

    PubMed  CAS  Google Scholar 

  • Murao S, Okhuni K, Naganao M (1988) A novel thermostable S-PI (pepstatin Ac)—insensitive acid proteinase from thermophilic Bacillus novo sp. strain Mn-32. Agric Biol Chem 52:1029–1031

    Google Scholar 

  • Nakada T, Ikegami S, Chaen H, Kubota M, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y (1996a) Purification and characterization of thermostable maltooligosyl trehalose synthese from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biosci Biotechnol Biochem 60:263–266

    Article  PubMed  CAS  Google Scholar 

  • Nakada T, Ikegami S, Chaen H, Kubota M, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y (1996b) Purification and characterization of thermostable maltooligosyl trehalose trehalohydrolase from thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biosci Biotechnol Biochem 60:267–270

    Article  PubMed  CAS  Google Scholar 

  • Nakayama T, Tsuruoka N, Akai M, Nishino T (2000) Thermostable collagenolytic activity of a novel thermophilic isolate, Bacillus sp. Strain NTAP-1. J Biosci Bioeng 89:612–614

    Article  PubMed  CAS  Google Scholar 

  • Neilsen JE, Borchert TV, Vriend G (2001) The determinants of α-amylase pH-activity profiles. Protein Eng 14:505–512

    Article  Google Scholar 

  • Norris PR (1990) Microbial Mineral Recovery. In: Ehrlich HL, Brierley CL (eds) Acidophilic bacteria and their activity in mineral sulfide oxidation. McGraw-Hill, New York, pp 1–27

    Google Scholar 

  • Norris PR, Clark DA, Owen JP, Waterhouse S (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulfide-oxidizing bacteria. Microbiology 142:775–783

    Google Scholar 

  • Nouailler M, Bruscella P, Lojou E, Lebrun R, Bonnyfoy V, Guerlesquin F (2006) Structural analysis of the HiPIP from the acidophilic bacteria: Acidithiobacillus ferrooxidans. Extremophiles 10:191–198

    Article  PubMed  CAS  Google Scholar 

  • Oda K, Nakazima T, Terashita T, Suziki KA, Murao S (1987a) Purification and properties of an S-PI (Pepstatin Ac) insensitive carboxyl proteinase from a Xanthomonas sp. Bacterium. Agric Biol Chem 51:3073–3080

    Article  CAS  Google Scholar 

  • Oda K, Sugitani M, Fukuhara K, Murao S (1987b) Purification and properties of a pepstatin-insensitive carboxyl proteinase from a gram negative bacterium. Biochim Biophys Acta 923:463–469

    Article  PubMed  CAS  Google Scholar 

  • Page-Sharp M, Behm CA, Smith GD (1999) Involvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cynobacterial Scytonema species isolated from desert soil. Biochim Biophys Acta 1472:519–528

    Article  PubMed  CAS  Google Scholar 

  • Prescott M, Peek K, Daniel RM (1995) Characterization of a thermostable pepstatin-insensitive acid proteinase from a Bacillus sp. Int J Biochem 27:729–739

    Article  CAS  Google Scholar 

  • Rajagopalan TG, Stein WH, Moore S (1966) The inactivation of pepsin by diazoacetylnorleucine methyl ester. J Biol Chem 241:4295–4297

    PubMed  CAS  Google Scholar 

  • Ren-Long J, Wu J, Chaw S-M, Tsai C-W, Tsen S-D (1999) A novel species of thermoacidophilic archaeon, Sulfolobus yangmingensis sp. nov. Int J Syst Bacteriol 49:1809–1816

  • Richards AB, Krakowka S, Dexter LB, Schmid H, Wolterbeek AP, Waalkens-Berendsen DH, Shigoyuki A, Kurimoto M (2002) Trehalose: a review of properties, history of use and human tolerance and results of multiple safety studies. Food Chem Toxicol 40:871–898

    Article  PubMed  CAS  Google Scholar 

  • Richardson TH, Tan X, Frey G, Callen W, Cabell M, Lam D, Macomber J, Short JM, Robertson DE, Miller C (2002) A novel, high performance enzyme for starch liquefaction. Discovery and optimization of a low pH, thermostable alpha amylase. J Biol Chem 277:26501–26507

    Article  PubMed  CAS  Google Scholar 

  • Rolfsmeier M, Haseltine C, Bini E, Clark A, Blum P (1998) Molecular characterization of the α-glucosidase gene (malA) from the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 180:1287–1295

    PubMed  CAS  Google Scholar 

  • Romonsellez F, Orell A, Jerez CA (2006) Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiology 152:59–66

    Article  CAS  Google Scholar 

  • Rubin-Pitel SB, Zhao H (2006) Recent advances in biocatalysis by directed enzyme evolution. Comb Chem High Throughput Screen 9:247–257

    Article  PubMed  CAS  Google Scholar 

  • Ruepp A, Graml W, Santos-Martinez ML, Koretke KK, Volker C, Mewes WH, Freishman D, Stocker S, Lupas NA, Baumeister W (2000) The genome sequence of thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407:508–513

    Article  PubMed  CAS  Google Scholar 

  • Sajedi RH, Naderi-Mahesh H, Khajeh K, Ahmadvand R, Ranjbar BA, Asoodeh A, Moradian F (2005) A calcium independent α-amylase that is active and stable at low pH from the Bacillus sp. KR-8104. Enzym Microbiol Technol 36:666–671

    Article  CAS  Google Scholar 

  • Schafer K, Magnusson U, Scheffel AS, Sandgren MOJ, Diederichs K, Welte W, Hulsmann A, Schneider E, Mowbray SL (2004) X-ray structures of the maltose maltodextrin binding protein of the thermoacidophilic bacterium Alicyclobacillus acidocaldarius provide insight into acidostability of the proteins. J Mol Biol 335:261–274

    Article  PubMed  CAS  Google Scholar 

  • Schelert J, Dixit V, Hoang V, Simbahan J, Drozda M, Blum P (2004) Occurence and characterizaton of mercury resistance in the hyperthermophilic archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186:427–437

    Article  PubMed  CAS  Google Scholar 

  • Schelert J, Drozda M, Dixit V, Dillman A, Blum P (2006) Regulation of mercury resistance in the crenarchaeote Sulfolobus solfataricus. J Bacteriol 188:7141–7150

    Article  PubMed  CAS  Google Scholar 

  • Schepers B, Thiemann V, Antranikian G (2006) Characterization of a novel glucoamylase from the thermoacidophilic archaeon Picrophilus torridus heterologously expressed in E. coli. Eng Life Sci 6:311–317

    Article  CAS  Google Scholar 

  • Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U (1995) Picrophilus gen. nov., fam. Nov. a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177:7050–7059

    PubMed  CAS  Google Scholar 

  • Schwermann B, Pfau K, Liliensiek B, Schleyer M, Fischer T, Bakker EP (1994) Purification, properties and structural aspects of the thermoacidophilic α-amylase from Alicyclobacillus acidocaldarius ATCC 27009. Insight into acidostability of proteins. Eur J Biochem 226:981–991

    Article  PubMed  CAS  Google Scholar 

  • Segerer A, Langworthy TA, Stetter KO (1988) Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from solfatara fields. Syst Appl Microbiol 10:161–171

  • Segerer A, Neuner A, Kristjansson JK, Stetter KO (1986) Acidanus infermus gen. nov., sp. nov., and Acidanus brierleyi comb. nov.: facultatively aerobic, extremely acidophlic thermophilic sulphur-metabolizing archaebacteria. Int J Syst Bacteriol 36:559–564

    Article  Google Scholar 

  • Segerer A, Stetter KO, Klink F (1985) Two contrary modes of chemolithotrophy in the same archaebacterium. Nature 313:787–789

    Article  PubMed  CAS  Google Scholar 

  • Segerer A, Trincone A, Gahrtz M, Stetter KO (1991) Stygiolobus azoricus gen. nov. represents a novel genus of anaerobic, extremely thermoacidophilic archaea of the order Sulfolobales. Int J Syst Bacteriol 41:495

    Article  Google Scholar 

  • Sen S, Dasu VV, Mandal B (2007) Development in directed evolution for improving enzyme functions. Appl Biochem Biotechnol 143:212–223

    Article  PubMed  CAS  Google Scholar 

  • Serour E, Antranikian G (2002) Novel thermoactive glucamylases from the thermoacidophilic Archaea Thermoplasma acidophilum, Picrophilus torridus and Picrophilus oshimae. Antonie Van Leewenhock 81:73–83

    Article  CAS  Google Scholar 

  • Sharma A, Satyanarayana T (2010) High maltose-forming, Ca2+-independent and acid stable α-amylase from a novel acidophilic bacterium Bacillus acidicola TSAS1. Biotechnol Lett 32:1503–1507

    Article  PubMed  CAS  Google Scholar 

  • Sharma A, Satyanarayana T (2011) Optimization of medium components and cultural variables for enhanced production of acidic high maltose-forming and Ca2+-independent α-amylase by Bacillus acidicola. J Biosci Bioeng 111:550–553

    Article  PubMed  CAS  Google Scholar 

  • She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC, Clausen IG, Curtis BA, De Moors A, Erauso G, Fletcher C, Gordon PM, 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, Vander OJ (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci USA 98:7835–7840

    Article  PubMed  CAS  Google Scholar 

  • Tang J (1971) Specific and irreversible inactivation of pepsin by substrate-like epoxides. J Biol Chem 246:4510–4517

    PubMed  CAS  Google Scholar 

  • Toogood SH, Prescott M, Daniel MR (1995) A pepstatin-insensitive aspartic proteinase from a thermophilic Bacillus sp. Biochem J 307:783–789

    PubMed  CAS  Google Scholar 

  • Tsuruoka N, Nakayama T, Ashida M, Hemmi H, Nakao M, Minakata H, Oyama H, Oda K, Nishino T (2003) Collagenolytic serine-carboxyl proteinase from Alicyclobacillus sendaiensis strain NTAP-1: purification, characterization, gene cloning and heterologous expression. Appl Environ Microbiol 69:162–169

    Article  PubMed  CAS  Google Scholar 

  • Verhaert RM, Beekwilder J, Olsthoorn R, Van DJ, Quax WJ (2002) Phage display selects for amylases with improved low pH starch binding. J Biotechnol 96:103–118

    Article  PubMed  CAS  Google Scholar 

  • Vossenberg JL, Driessen AJ, Zillig W, Konings WN (1998) Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Picrophilus oshimae. Extremophiles 2:67–74

    Article  PubMed  Google Scholar 

  • Wakao N, Hiraishi A, Nagasawa N, Matsuura T, Matsumoto T, Sakurai Y, Shiota H (1994) Acidiphilium multivorum sp. nov., an acidophilic chemoorganotrophic bacterium from pyritic acid mine drainage. J Gen Appl Microbiol 40:143–159

    Article  CAS  Google Scholar 

  • Wichlacz PL, Unz RF, Langworthy TA (1986) Acidiphilium angustum sp. nov., Acidiphilium facilis sp. nov., Acidiphilium rubrum sp. nov. Acidophilic heterotrophic bacteria isolated from acidic coal mine drainage. Int J Syst Bacteriol 36:197–201

    Article  Google Scholar 

  • Wisotzkey JD, Jurtshuk P, Fox GE, Deinhard G, Poralla K (1992) Comparative sequence analyses on the 16S ribosomal-RNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris, and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. Int J Syst Bacteriol 42:263–269

    Article  PubMed  CAS  Google Scholar 

  • Worthington P, Hoang V, Perez-Pomares F, Blum P (2003) Targeted disruption of the α-amylase gene in the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 185:482–488

    Article  PubMed  CAS  Google Scholar 

  • Xiang X, Dong X, Huang L (2003) Sulfolobus tengchongensis sp. nov., a novel thermoacidophilic archaeaon isolated from a hot spring in Tengchong, China. Extremophiles 7:493–498

    Article  PubMed  CAS  Google Scholar 

  • Yamashiro K, Yokobori S, Oshima TE, Yamagishi A (2006) Structural analysis of the plasmid pTA1 isolated from the thermoacidophilic archaeon Thermoplasma acidophilum. Extremophiles 10:327–335

    Article  PubMed  CAS  Google Scholar 

  • Yasuda M, Yamagishi A, Oshima T (1995) The plasmids found in isolates of the acidothermophilic archaebacterium Thermoplasma acidophilum. FEMS Microbiol Lett 128:157–162

    Article  CAS  Google Scholar 

  • Zhao Q, Liu H, Zhang Y, Zhang Y (2010) Engineering of protease-resistant phytase from Penicillium sp.: high thermal stability, low optimal temperature and pH. J Biosci Bioeng 110:638–645

    Article  PubMed  CAS  Google Scholar 

  • Zillig W, Boeck A (1987) In Validation of the publication of new names and new combinations previously effectively published outside the IJSB. List No. 23. Int J Syst Bacteriol 37:179–180

    Article  Google Scholar 

  • Zillig W, Stetter KO, Wunderl S, Schultz W, Priess H, Scholz I (1980) In Validation of the publication of new names and new combinations previously effectively published outside the IJSB. List No. 5. Int J Syst Bacteriol 30:676–677

    Article  Google Scholar 

  • Zillig W, Yeats S, Holz I, Boeck A, Rettenberger M, Gropp F, Simon G (1986) Desulfurolobus ambivalens, gen. nov., sp. nov., an autotrophic archaebacterium facultatively oxidizing or reducing sulphur. Syst Appl Microbiol 8:197–203

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India

    Archana Sharma & T. Satyanarayana

  2. New Energy and Industrial Technology Development Organization (NEDO), 19F Muza Kawasaki Building, 1310 Omiya-cho, Saiwai-ku, Kawasaki, Kanagawa, 212-8554, Japan

    Yutaka Kawarabayasi

Authors
  1. Archana Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yutaka Kawarabayasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Satyanarayana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Satyanarayana.

Additional information

Communicated by S. Albers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, A., Kawarabayasi, Y. & Satyanarayana, T. Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16, 1–19 (2012). https://doi.org/10.1007/s00792-011-0402-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-011-0402-3

Keywords

Search

Navigation