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Distribution of Acidophilic Microorganisms in Natural and Man- Made Acidic Environments Sabrina Hedrich and Axel Schippers*

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Distribution of Acidophilic Microorganisms in Natural and Man- Made Acidic Environments Sabrina Hedrich and Axel Schippers* Distribution of Acidophilic Microorganisms in Natural and Man- made Acidic Environments Sabrina Hedrich and Axel Schippers* Federal Institute for Geosciences and Natural Resources (BGR), Resource Geochemistry Hannover, Germany *Correspondence: [email protected] https://doi.org/10.21775/cimb.040.025 Abstract areas, or environments where acidity has arisen Acidophilic microorganisms can thrive in both due to human activities, such as mining of metals natural and man-made environments. Natural and coal. In such environments elemental sulfur acidic environments comprise hydrothermal sites and other reduced inorganic sulfur compounds on land or in the deep sea, cave systems, acid sulfate (RISCs) are formed from geothermal activities or soils and acidic fens, as well as naturally exposed the dissolution of minerals. Weathering of metal ore deposits (gossans). Man-made acidic environ- sulfdes due to their exposure to air and water leads ments are mostly mine sites including mine waste to their degradation to protons (acid), RISCs and dumps and tailings, acid mine drainage and biomin- metal ions such as ferrous and ferric iron, copper, ing operations. Te biogeochemical cycles of sulfur zinc etc. and iron, rather than those of carbon and nitrogen, RISCs and metal ions are abundant at acidic assume centre stage in these environments. Ferrous sites where most of the acidophilic microorganisms iron and reduced sulfur compounds originating thrive using iron and/or sulfur redox reactions. In from geothermal activity or mineral weathering contrast to biomining operations such as heaps provide energy sources for acidophilic, chemo- and bioleaching tanks, which are ofen aerated to lithotrophic iron- and sulfur-oxidizing bacteria and enhance the activities of mineral-oxidizing prokary- archaea (including species that are autotrophic, otes, geothermal and other natural environments, heterotrophic or mixotrophic) and, in contrast to can harbour a more diverse range of acidophiles most other types of environments, these are ofen including obligate anaerobes. numerically dominant in acidic sites. Anaerobic growth of acidophiles can occur via the reduction of ferric iron, elemental sulfur or sulfate. While the Populations in natural acidic activities of acidophiles can be harmful to the envi- environments ronment, as in the case of acid mine drainage, they Environments where acid is formed naturally with- can also be used for the extraction and recovery of out the infuence of mining include geothermal metals, as in the case of biomining. Considering terrestrial sites (solfatara) that occur at active volca- the important roles of acidophiles in biogeochemi- noes, deep-sea hydrothermal systems, and naturally cal cycles, pollution and biotechnology, there is a exposed sulfde ore deposits. Tese sites are of great strong need to understanding of their physiology, interest when searching for organisms to be used, biochemistry and ecology. for example in biomining operations, as it is ofen the case that these environments have existed for many years and therefore indigenous microorgan- Introduction isms are potentially adapted to high metal and salt Environments inhabited by acidophiles can be of concentrations, extreme temperature and low pH natural origin where acidic conditions have existed (Table 10.1). for many years, such as volcanic or geothermal caister.com/cimb 25 Curr. Issues Mol. Biol. Vol. 40 Hedrich and Schippers Table 10.1 Physico-chemical parameters and prokaryotic diversity of selected natural environments where acidophiles have been detected Temperature Site pH (°C) Bacteria Archaea Reference Geothermal sites Yellowstone 2.0– 30–90 Fx. thermotolerans, Ad. brierleyi, Sulfolobales, Johnson et al. National Park, 4.4 Sulfobacillus-like, Thermoproteales, (2003), Inskeep et Wyoming, Am. ferrooxidans-like, Desulforococales, al. (2004, 2010), USA Methylobacterium- ‘Geoarchaeota’, Kozubal et al. like, Acidisphaera sp., Thaumarchaeota, (2013), Beam et Alicyclobacillus-like, H. Metallosphaera-like, al. (2014) acidophilus, Thiomonas sp. Marinithermus sp. Montserrat, 1.6– 24–99 At. caldus, At. ferrooxidans. Sulfolobus spp., Acidianus Atkinson et al. Lesser Antilles 7.4 L. ferrooxidans, Am. spp., Ferroplasma-like (2000), Burton ferrooxidans, Sulfobacillus and Norris (2000) spp., Acidiphilium-like, Alicyclobacillus spp., Desulfosporosinus sp. St. Lucia, 2.0 42.6 At. caldus, Sulfobacillus Acidianus spp., unknown Stout et al. (2009) Lesser Antilles spp. Eukaryota Palaeochori 2.0 50–60 At. caldus, Acidianus spp., Norris (2011) Bay, Milos ‘Acidithiomicrobium’, Ferroplasma-like Acidithiobacillus spp., Sulfobacillus spp. Vulcano, Italy 2.0– 35–75 Acidithiobacillus spp., T. Tp. volcanium, Ad. brierleyi, Simmons and 3.5 prosperus Ad. inferno Norris (2002) Mutnovsky 3.5– 70 At. caldus, Thermotogae Thaumarchaeota, Wemheuer et al. volcano, 4.0 Acidilobus sp., Vulcanisaeta (2013) Kamchatka sp., Thermoplasma sp. Hveragerji, 2.5– 81–90 NR Sulfolobales, Kvist et al. (2007) Iceland 3.5 8–20 Sulfobacillus spp., Thermoproteales, Davis-Belmar Salar de 1.1– Alicyclobacillus crenarchaeotal group I.1b et al. (2013), Gorbea 4.8 spp., Acidisoma sp., Thermoplastales, Escudero et al. Alkalibacter sp., Proteo- Thermococcales, (2013) and Actinobacteria, Halobacteriales, Cyanobacteria Methanosarcinales and Methanobacteriales, Thermoproteales Copahue <1.0– 8–85 At. ferrooxidans, At. Ferroplasma spp., Ad. Urbieta et al. volcanic area 4.0 thiooxidans, Leptospirillum copahuensis, Sulfolobus (2012, 2014a) including spp., At. caldus-like, spp. Rio Agrio, Sulfobacillus spp. Argentina Deep sea hydrothermal vents deep sea vent, 3–6 50–80 NR ‘Aciduliprofundum boonei’ Reysenbach et al. Eastern Lau (2006) Spreading Centre Caves Frasassi cave, 0–1.5 13 At. thiooxidans, Ferroplasma spp., Macalady (2007), Italy Sulfobacillus spp., Am. ‘G-plasma’ Jones (2012) ferrooxidans Cueva de Villa 1.4 28 Acidithiobacillus spp., Am. NR Hose et al. (2000) Luz, Mexico ferrooxidans caister.com/cimb 26 Curr. Issues Mol. Biol. Vol. 40 Distribution of Acidophiles in the Environment Table 10.1 Continued Temperature Site pH (°C) Bacteria Archaea Reference Gossan Citronen Fjord, 1.9– 2–5 Acidithiobacillus-like, NR Langdahl and Greenland 2.5 heterotrophs Ingvorsen (1997) Antarctica 3.2– 0–4 T. plumbophilus, At. NR Dold et al. (2013) 4.5 ferrivorans Abbreviations: Acidianus (Ad.), Acidilobus (Al.), Acidimicrobium (Am.), Acidiphilium (A.), Acidisphaera (As.), Acidithiobacillus (At.), ‘Acidithiomicrobium’ (Atm.), Alicyclobacillus (Alb.), Ferrithrix (Fx.), Ferroplasma (Fp.), Hydrogenobaculum (H.), Leptospirillum (L.), Metallosphaera (M.), Picrophilus (P.), Sulfsphaera (Ss.), Sulfobacillus (Sb.), Sulfolobus (S.), Thermoplasma (Tp.), Thiobacillus (T.). NR, not reported. Te frst sulfur-metabolizing archaeon, subse- Hydrothermal environments quently named as Acidianus brierleyi, was isolated Solfatara are characterized by high temperatures by James Brierley in 1965 from geothermal sites in (up to 100°C) and elevated concentrations of sulfur Yellowstone (Brierley, 1973). Further cultivation- (and RISCs), hydrogen and ofen also soluble based studies on acidophiles from YNP resulted in metals and arsenic. When elemental sulfur, formed the enrichment of novel thermophilic iron- and/ by the condensation of volcanic gases such as H2S or sulfur-metabolizing and heterotrophic bacteria and SO2, is oxidized by acidophilic prokaryotes, (Johnson et al., 2003), including the isolation of the sulfuric acid is formed which results in low-pH type strain of the acidophilic, moderately thermo- environments. Owing to the low pH and high philic species Ferrithrix thermotolerans (Johnson et temperatures in volcanic areas, acid-labile minerals al., 2009) and Acidicaldus organivorans (Johnson et are dissolved and release elevated concentration al., 2006). of transition metals and metalloids. Te nature of While a number of described acidophilic hydrothermal sites is dictated by the subterranean archaeal species have been detected in samples geology and water fow. In particular, the degree of YNP, several studies have shown that the hot of mixing of deep hydrothermally heated water springs of YNP are a source of novel and deeply (bufered in the neutral–alkaline region by CO2/ branching archaea (e.g. Beam et al., 2014; Inskeep – HCO3 ) with cold shallow groundwater (strongly et al., 2010, 2004; Table 10.1). Archaea in an acidic acidifed by microbial and chemical oxidation iron oxide geothermal spring were further analysed of sulfur compounds) determines pH and tem- by Kozubal et al. (2013) and proposed as a new can- perature of the environment (Atkinson, 2000). Te didate phylum within the domain Archaea referred microbiology of acidic geothermal areas has been to as ‘Geoarchaeota’ or ‘novel archaeal group 1 studied for more than four decades (e.g. Johnson (NAG1)’. Tese organisms were found to contain et al., 2003; Brock, 2001; 1978) and microbial pathways necessary for the catabolism of peptides communities in these environments host a variety and complex carbohydrates and genes involved in of deeply rooted known and unknown Archaea, the metabolism of oxygen. Furthermore Beam et al. Bacteria and Eukarya. (2014) applied metagenome sequence analysis to One of the most intensively studied natural study thermophilic populations (65–72°C) at acidic acidic hydrothermal environment is Yellowstone iron oxide- and sulfur-rich sediment environments National Park (YNP; Wyoming, USA) which of YNP. Tese deeply rooted Taumarchaeota were houses the most
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