Acidophiles

Abstract

Microorganisms growing in highly acidic environments (pH values below 3) are found in all three domains of life: Archaea, Bacteria and Eucarya. Such organisms thrive in acidic sulfur springs and in association with mining activities where microbial oxidation of pyrite and other reduced sulfur compounds lead to the formation of sulfuric acid. Acidophilic prokaryotes are also involved in the industrial leaching of copper and other metals from ores. Some acidophiles grow at high temperatures. Physiologically, the acidophiles are very diverse: there are aerobic and facultative anaerobic chemolithotrophs and different types of heterotrophic prokaryotes, photoautotrophic eukaryotes, predatory protozoa and others. Acidophilic microorganisms maintain their intracellular pH close to neutrality and their cytoplasmic membrane may support proton gradients up to five orders of magnitude; their membrane potential is often reversed in comparison with neutrophiles and alkaliphiles, with an intracellular positive charge.

Key concepts:

  • Microbial life is possible in strongly acidic environments and even at pH values below zero.

  • The low pH of highly acidic environments in volcanic areas and environments associated with metal ore mining is caused by the activities of acidophilic microorganisms that oxidize reduced sulfur compounds to sulfuric acid.

  • Acidophilic microorganisms are found in all three domains of life: Archaea, Bacteria and Eucarya.

  • Unicellular eukaryotic green algae such as Dunaliella acidophila and Chlamydomonas acidophila perform photosynthesis at pH values down to 0–1 and the red alga Cyanidium caldarium grows as a photoautotroph in acidic hot springs up to 57°C and at pH<2–4.

  • Some thermoacidophilic Archaea thrive at low pH up to very high temperatures. Sulfolobus and Acidanus spp. grow up to 96°C at pH 1–5; Picrophilus oshimae tolerates pH<0 and grows up to 65°C.

  • Acidophilic microorganisms keep their intracellular pH at values close to neutrality and maintain a proton gradient over their cytoplasmic membranes of up to five orders of magnitude.

  • In contrast to neutrophilic and alkaliphilic microorganisms that maintain an outside‐positive membrane potential, the membrane potential over the cytoplasmic membrane can be reversed, positive‐inside, in acidophilic microorganisms.

  • Extracellular enzymes of acidophilic microorganisms are optimally active at low pH.

  • Acid mine drainage is caused by the chemolithotrophic oxidation of pyrite and other reduced sulfur compounds in the ores by acidophilic prokaryotes such as Acidithiobacillus, Leptospirillum and Ferroplasma.

  • The activities of the same types of organisms that cause acid mine drainage are exploited industrially for the bioleaching of copper and other metals from ores.

Keywords: Acidithiobacillus; Acid mine drainage; Acidophiles; Metal leaching; Sulfolobus; Thermoacidophiles

Figure 1.

The red waters (pH∼2) of the Rio Tinto, Spain, coloured red by jarosite [HFe3(SO4)2(OH)6] formed by chemolithotrophic iron‐ and sulfur‐oxidizing prokaryotes. Photograph: Extremophiles Lab, CAB, Madrid.

Figure 2.

A simplified scheme showing interactions of the pH gradient, substrate oxidation and ATP synthesis in iron‐oxidizing Acidithiobacillus ferrooxidans, with electrons from ferrous iron involved in proton removal in the cytoplasm after transport via cytochromes (cyt) and rusticyanin (ru).

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References

Amaral‐Zettler LA, Gómez F, Zettler E et al. (2002) Eukaryotic diversity in Spain's River of Fire. Nature 417: 137.

Baker BJ and Banfield JF (2003) Microbiology in acid mine drainage. FEMS Microbiology Ecology 44: 139–152.

Baker BJ, Lutz MA, Dawson SC, Bond PL and Banfield JF (2004) Metabolically active eukaryotic communities in extremely acidic mine drainage. Applied and Environmental Microbiology 70: 6264–6271.

Baker BJ, Tyson GW, Goosherst L and Banfield JF (2009) Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Applied and Environmental Microbiology 75: 2192–2199.

Baumgartner M, Eberhardt S, de Jonckheere JF and Stetter KO (2009) Tetramitus thermacidophilus n. sp., an amoeboflagellate from acidic hot springs. Journal of Eukaryotic Microbiology 56: 201–206.

Beardall J and Entwisle L (1984) Internal pH of the obligate acidophile Cyanidium caldarium Geitler (Rhodophyta?). Phycologia 23: 397–399.

Bond P, Smriga SP and Banfield JF (2000) Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm in an extreme acid mine drainage site. Applied and Environmental Microbiology 66: 3842–3849.

Chen L, Brugger K, Skovgaard M et al. (2005) The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. Journal of Bacteriology 187: 4992–4999.

Doemel WN and Brock TD (1971) The physiological ecology of Cyanidium caldarium. Journal of General Microbiology 67: 17–32.

Dopson M, Baker‐Austin C, Hind A, Bowman JP and Bond PL (2004) Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Applied and Environmental Microbiology 70: 2079–2088.

Enami E, Akutsu H and Kyogoku Y (1986) Intracellular pH regulation in an acidophilic unicellular alga, Cyanidium caldarium: 31P‐NMR determination of intracellular pH. Plant and Cell Physiology 27: 1351–1359.

Foster JW (2004) E. coli acid resistance: tales of an amateur acidophile. Nature Reviews in Microbiology 2: 898–907.

Fütterer O, Angelov H, Lisegang H et al. (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proceedings of the National Academy of Sciences of the USA 101: 9091–9096.

Gimmler H, Weis U, Weiss C, Kugel H and Treffny B (1989) Dunaliella acidophila (Kalina) Masyuk: an alga with a positive membrane potential. New Phytologist 113: 175–184.

Goltsman DSA, Denef VJ, Singer SW et al. (2009) Community genomic and proteomic analyses of chemoautotrophic iron‐oxidizing “Leptospirillum rubarum” (group II) and “Leptospirillum ferrodiazotrophicum” (group III) bacteria in acid mine drainage. Applied and Environmental Microbiology 75: 4599–4615.

González‐Toril E, Gómez F, Malki M and Amils R (2006) The isolation and study of acidophilic microorganisms. In: Rainey F and Oren A (eds) Methods in Microbiology, vol. 35. Extremophiles, pp. 471–510. Amsterdam, The Netherlands: Elsevier/Academic Press.

Goodwin S and Zeikus JG (1987) Physiological adaptations of anaerobic bacteria to low pH: metabolic control of proton motive force in Sarcina ventriculi. Journal of Bacteriology 169: 2150–2157.

Gross S and Robbins EI (2000) Acidophilic and acid‐tolerant fungi and yeasts. Hydrobiologia 433: 91–109.

Gross W (2000) Ecophysiology of algae living in highly acidic environments. Hydrobiologia 433: 31–37.

Hallman R, Friedrich A, Koops H‐P et al. (1992) Physiological characteristics of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans and physiochemical factors influence microbial metal leaching. Geomicrobiology Journal 10: 193–206.

Ingledew WJ (1982) Thiobacillus ferrooxidans: the bioenergetics of an acidophilic chemolithotroph. Biochimica et Biophysica Acta 683: 89–117.

Johnson DB and Hallberg KB (2003) The microbiology of acidic mine waters. Research in Microbiology 154: 466–473.

Johnson DB and Hallberg KB (2009) Carbon, iron and sulfur metabolism in acidophilic micro‐organisms. Advances in Microbial Physiology 54: 201–255.

Johnson DB, Bacelar‐Nicolau P, Okibe N, Thomas A and Hallberg KB (2009) Ferrimicrobium acidiphilum gen. nov., sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron‐oxidizing, extremely acidophilic actinobacteria. International Journal of Systematic and Evolutionary Microbiology 59: 1082–1089.

Kawarabayashi Y, Hino Y, Horikawa H et al. (2001) Complete genome sequence of an anaerobic crenarchaeon, Sulfolobus tokudaii strain 7. DNA Research 8: 123–140.

Kimura S, Hallberg KB and Johnson DB (2006) Sulfidogenesis in low pH (3.8–4.2) media by a mixed population of acidophilic bacteria. Biodegradation 17: 57–65.

López‐Archilla AL, Marin I and Amils R (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microbial Ecology 41: 20–35.

Matin A (1990) Keeping a neutral cytoplasm: the bioenergetics of obligate acidophiles. FEMS Microbiology Reviews 75: 307–318.

Matzke J, Schwermann B and Bakker EP (1997) Acidostable and acidophilic proteins: the example of the α‐amylase from Alicyclobacillus acidocaldarius. Comparative Biochemistry and Physiology A 118: 475–479.

Messerli MA, Amaral‐Zettler LA, Zettler E et al. (2005) Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile. Journal of Experimental Biology 208: 2569–2579.

Packroff G and Woelfl S (2000) A review on the occurrence and taxonomy of heterotrophic protists in extreme acidic environments of pH values ≤3. Hydrobiologia 433: 153–156.

Pick U (1999) Dunaliella acidophila – a most extreme acidophilic alga. In: Seckbach J (ed.) Enigmatic Microorganisms and Life in Extreme Environments, pp. 467–478. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Rawlings DE, Tributsch H and Hansford GS (1999) Reasons why ‘Leptospirillum’‐like species rather than Thiobacillus ferrooxidans are the dominant iron‐oxidizing bacteria in many commercial processes for the biooxidation of pyrite and related ores. Microbiology 145: 5–13.

Remis D, Simonis W and Gimmler H (1992) Measurement of transmembrane electric potential of Dunaliella acidophila by microelectrodes. Archives of Microbiology 158: 350–355.

Reysenbach AL, Liu Y, Banta AB et al. (2006) A ubiquitous thermoacidophilic archaeon from deep‐sea hydrothermal vents. Nature 442: 444–447.

Ruepp A, Graml W, Santos‐Martinez ML et al. (2000) The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407: 508–513.

Schäfer K, Magnusson U, Scheffel F et al. (2004) X‐ray structures of the maltose‐maltodextrin‐binding protein of the thermoacidophilic bacterium Aclicyclobacillus acidocaldarius provide insight into acid stability of proteins. Journal of Molecular Biology 335: 261–274.

Schleper C, Puehler G, Kühlmorgen B and Zillig W (1995) Life at extremely low pH. Nature 375: 741–742.

Schrenk MO, Edwards KJ, Goodman RM, Hamers RJ and Banfield JF (1998) Distribution of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans: implications for generation of acid mine drainage. Science 279: 1519–1522.

Schwermann B, Pfau K, Liliensiek B et al. (1994) Purification, properties and structural aspects of a thermoacidophilic α‐amylase from Alicyclobacillus acidocaldarius ATCC 27009. European Journal of Biochemistry 226: 981–991.

Segerer A, Langworthy TA and Stetter KO (1988) Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from solfatara fields. Systematic and Applied Microbiology 10: 161–171.

Segerer A, Neuner A, Kristjansson JK and Stetter KO (1986) Acidianus infernus gen. nov., sp. nov., and Acidianus brierleyi comb. nov.: facultatively aerobic, extremely acidophilic thermophilic sulfur‐metabolizing archaebacteria. International Journal of Systematic Bacteriology 36: 559–564.

She Q, Singh RK, Confalonieri E et al. (2001) The genome of the crenarchaeon Sulfolobus solfataricus P2. Proceedings of the National Academy of Sciences of the USA 98: 7835–7840.

Stingl K, Uhlemann EM, Schmid R, Altendorf K and Bakker EP (2002) Energetics of Helicobacter pylori and its implications for the mechanism of urease‐dependent acid tolerance at pH 1. Journal of Bacteriology 184: 3053–3060.

Tyson GW, Chapman J, Hugenholtz P et al. (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37–43.

Tyson GW, Lo I, Baker BJ et al. (2005) Genome‐directed isolation of the key nitrogen‐fixer Leptospirillum ferrodiazotrophum sp. nov. from an acidophilic microbial community. Applied and Environmental Microbiology 71: 6319–6324.

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

Waksman SA and Joffe JS (1922) Microörganisms concerned in the oxidation of sulfur in the soil. II. Thiobacillus thiooxidans, a new sulfur‐oxidizing organism in the soil. Journal of Bacteriology 7: 239–256.

Wilmes P, Remis JP, Hwang M et al. (2009) Natural acidophilic biofilm communities reflect distinct organismal and functional organization. ISME Journal 3: 266–270.

Zychlinsky E and Matin A (1983) Cytoplasmic pH homeostasis in an acidophilic bacterium, Thiobacillus acidophilus. Journal of Bacteriology 156: 1352–1355.

Further Reading

Angelov A and Liebl W (2007) Genomics of acidophiles. In: Gerdes C and Glansdorff N (eds) Physiology and Biochemistry of Extremophiles, pp. 279–292. Washington DC: ASM Press.

Franke S and Rensing C (2007) Acidophiles: mechanisms to tolerate metal and acid toxicity. In: Gerdes C and Glansdorff N (eds) Physiology and Biochemistry of Extremophiles, pp. 271–278. Washington DC: ASM Press.

Goebel BM, Norris PR and Burton NP (2000) Acidophiles in biomining. In: Priest FG and Goodfellow M (eds) Applied Microbial Systematics, pp. 293–314. Dordrecht, The Netherlands: Kluwer Academic Publishers.

González‐Toril E, Llobet‐Brossa E, Casamayor EO, Amann R and Amils R (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Applied and Environmental Microbiology 69: 4855–4865.

Hallberg KB and Johnson DB (2001) Biodiversity of acidophilic prokaryotes. Advances in Applied Microbiology 49: 37–84.

Johnson DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiology Ecology 27: 307–317.

Johnson DB (2007) Physiology and ecology of acidophilic microorganisms. In: Gerdes C and Glansdorff N (eds) Physiology and Biochemistry of Extremophiles, pp. 257–270. Washington DC: ASM Press.

Norris PR and Ingledew WJ (1992) Acidophilic bacteria: adaptations and applications. In: Herbert RA and Sharp RJ (eds) Molecular Biology and Biotechnology of Extremophiles, pp. 115–142. Glasgow, UK: Blackie.

Norris PR and Johnson DB (1998) Acidophilic microorganisms. In: Horikoshi K and Grant WD (eds) Extremophiles: Microbial Life in Extreme Environments, pp. 133–153. New York: Wiley‐Liss.

Seckbach J (ed.) (1994) Evolutionary pathways and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells. Dordrecht, The Netherlands: Kluwer Academic Publishers.

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Oren, Aharon(Mar 2010) Acidophiles. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000336.pub2]