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Chapter 4.3.1 : The Microbiology of Extremely Acidic Environments

Authors: D. Barrie Johnson1, Angeles Aguilera2
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Affiliations: 1: College of Natural Sciences, Bangor University, Deiniol Road, Bangor, LL57 2UW, UK; 2: Centro de Astrobiología (INTA-CSIC), Carretera de Ajalvir Km4, 28850 Madrid, Spain
Content Type: Reference
Publication Year: 2016

Category: Environmental Microbiology

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Abstract:

Extremely acidic environments, defined having a pH of <3, are found in locations as diverse as the Arctic and the Tropics. While these be natural phenomena, human activity, most notoriously mining of metals and coals, are often responsible for the severe acidification of localized environments. The indigenous microflora in extremely acidic environments include species of prokaryotes and eukaryotes, many of which are obligately acidophilic. Acidophiles are widely distributed throughout the "tree of life", and include species of Bacteria, Archaea and Eukarya that are often only very distantly related to each other. Various mechanisms are used by acidophiles to adapt to the challenges they face, which include contending with elevated concentrations of transition metals and metalloids, and severely limited bioavailability of macronutrients such as phosphate.

Inorganic energy sources (reduced iron and sulfur) are highly abundant in many extremely acidic environments. Chemolithotrophic acidophiles are the basis of food webs in subterranean and also contribute to net primary production in deep submarine geothermal vents. However, where solar energy is available phototrophic acidophiles, predominantly species of acidophilic eukaryotic microalgae, proliferate and assume the dominant role of primary producers. Acidophilic microorganisms interact with each other in various ways, including via redox transformations of iron and sulfur, generating electron donors and acceptors for prokaryotic metabolisms, and via provision of organic compounds (supporting heterotrophic species) or inorganic carbon (supporting autotrophs). Acidophiles have long been used to extract metals from ores (biomining) and biotechnologies are emerging that harness their abilities to remediate polluted waters and recover metals.

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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The Microbiology of Extremely Acidic Environments
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Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
/content/10.1128/9781555818821.ch4.3.1.ch4.3.1fig01
FIGURE 1

Acidic environments at geothermal sites: (a) Norris geyser basin, Yellowstone National Park, WY; (b) a hot spring on São Miguel, Azores; (c) prismatic sulfur crystals forming in a volcanic vent, Montserrat, WI. doi:10.1128/9781555818821.ch4.3.1.f1

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FIGURE 1

Acidic environments at geothermal sites: (a) Norris geyser basin, Yellowstone National Park, WY; (b) a hot spring on São Miguel, Azores; (c) prismatic sulfur crystals forming in a volcanic vent, Montserrat, WI. doi:10.1128/9781555818821.ch4.3.1.f1

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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FIGURE 2

Simplified representation of ferrous iron oxidation by the iron-oxidizing acidithiobacilli protons entering the cytoplasm via the membrane-bound ATP synthetase complex (ATPase, shown in purple) are counterbalanced by electrons that derive from the oxidation of ferrous iron, mediated by cytochromes and rusticyanin (shown in green and yellow) located in the acidic periplasm. Cytochrome oxidase (shown in blue) catalyzes the reduction of molecular oxygen by incoming protons and electrons, generating water, the sole metabolic end product of this process.

doi:10.1128/9781555818821.ch4.3.1.f2

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FIGURE 2

Simplified representation of ferrous iron oxidation by the iron-oxidizing acidithiobacilli protons entering the cytoplasm via the membrane-bound ATP synthetase complex (ATPase, shown in purple) are counterbalanced by electrons that derive from the oxidation of ferrous iron, mediated by cytochromes and rusticyanin (shown in green and yellow) located in the acidic periplasm. Cytochrome oxidase (shown in blue) catalyzes the reduction of molecular oxygen by incoming protons and electrons, generating water, the sole metabolic end product of this process.

doi:10.1128/9781555818821.ch4.3.1.f2

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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/content/10.1128/9781555818821.ch4.3.1.ch4.3.1fig03
FIGURE 3

Microbial eukaryotic biofilms found in the Río Tinto: (a) green filaments formed mainly by and ; (b) biofilms of sp.; (c) biofilms formed mostly by euglenoids and diatoms; biofilms of sp. The scale bars represent 5 cm. doi:10.1128/9781555818821.ch4.3.1.f3

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FIGURE 3

Microbial eukaryotic biofilms found in the Río Tinto: (a) green filaments formed mainly by and ; (b) biofilms of sp.; (c) biofilms formed mostly by euglenoids and diatoms; biofilms of sp. The scale bars represent 5 cm. doi:10.1128/9781555818821.ch4.3.1.f3

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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FIGURE 4

Light micrographs of different eukaryotic species isolated from the Río Tinto: (a) sp. (filamentous green algae); (b) sp. (Heliozoa); (c) sp. (red algae); (d) ; (e) amoebae (protoctista) (f) sp. (green algae). The scale bar represents 10 μm. doi:10.1128/9781555818821.ch4.3.1f4

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FIGURE 4

Light micrographs of different eukaryotic species isolated from the Río Tinto: (a) sp. (filamentous green algae); (b) sp. (Heliozoa); (c) sp. (red algae); (d) ; (e) amoebae (protoctista) (f) sp. (green algae). The scale bar represents 10 μm. doi:10.1128/9781555818821.ch4.3.1f4

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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/content/10.1128/9781555818821.ch4.3.1.ch4.3.1fig05
FIGURE 5

(Top): schematic representation of the “overlay” technique for isolating and enumerating different physiological groups of acidophilic prokaryotes. A two-layered gel is prepared, with the underlay being inoculated either with a strain (e.g., SJH) of (to cultivate autotrophic acidophiles), or (to cultivate heterotrophic acidophiles, as this acidophile “detoxifies” the medium but does not use organic compounds such as glycerol and yeast extract which are used by most other acidophilic heterotrophs). (Bottom): (a) colonies of iron-oxidizing acidophiles, isolated from the Río Tinto on ferrous iron overlay plates; (b) colonies of heterotrophic acidophiles, isolated from an abandoned copper mine (Roeros) in Norway on yeast extract–containing overlay plates. doi:10.1128/9781555818821.ch4.3.1.f5

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FIGURE 5

(Top): schematic representation of the “overlay” technique for isolating and enumerating different physiological groups of acidophilic prokaryotes. A two-layered gel is prepared, with the underlay being inoculated either with a strain (e.g., SJH) of (to cultivate autotrophic acidophiles), or (to cultivate heterotrophic acidophiles, as this acidophile “detoxifies” the medium but does not use organic compounds such as glycerol and yeast extract which are used by most other acidophilic heterotrophs). (Bottom): (a) colonies of iron-oxidizing acidophiles, isolated from the Río Tinto on ferrous iron overlay plates; (b) colonies of heterotrophic acidophiles, isolated from an abandoned copper mine (Roeros) in Norway on yeast extract–containing overlay plates. doi:10.1128/9781555818821.ch4.3.1.f5

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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/content/10.1128/9781555818821.ch4.3.1.ch4.3.1fig06
FIGURE 6

(a) the Río Tinto in the Iberian Peninsula Belt, Spain; (b) a pit lake in the abandoned São Domingos copper mine, Portugal. doi:10.1128/9781555818821.ch4.3.1.f6

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FIGURE 6

(a) the Río Tinto in the Iberian Peninsula Belt, Spain; (b) a pit lake in the abandoned São Domingos copper mine, Portugal. doi:10.1128/9781555818821.ch4.3.1.f6

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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/content/10.1128/9781555818821.ch4.3.1.ch4.3.1fig07
FIGURE 7

Microbial growth and geochemical transformations of iron, sulfur, and carbon in an acidic (pH 2.5) stream draining a small abandoned copper mine (Cantareras) in the Iberian Pyrite Belt. Algal surface streamers overlie a bacterial mat that is light brown in color (and populated by iron-reducing acidophiles) which in turn overlies a charcoal-colored mat, which contains sulfate-reducing and other heterotrophic acidophiles. Most fixation of inorganic carbon in the stream community is mediated by acidophilic algae, though autotrophic iron- and sulfur-oxidizing bacteria also contribute to net primary production. doi:10.1128/9781555818821.ch4.3.1.f7

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Image of FIGURE 7
FIGURE 7

Microbial growth and geochemical transformations of iron, sulfur, and carbon in an acidic (pH 2.5) stream draining a small abandoned copper mine (Cantareras) in the Iberian Pyrite Belt. Algal surface streamers overlie a bacterial mat that is light brown in color (and populated by iron-reducing acidophiles) which in turn overlies a charcoal-colored mat, which contains sulfate-reducing and other heterotrophic acidophiles. Most fixation of inorganic carbon in the stream community is mediated by acidophilic algae, though autotrophic iron- and sulfur-oxidizing bacteria also contribute to net primary production. doi:10.1128/9781555818821.ch4.3.1.f7

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
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Tables

The Microbiology of Extremely Acidic Environments
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Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
/content/10.1128/9781555818821.ch4.3.1.ch4.3.1tab01
TABLE 1

Comparison of free energy changes associated with the oxidation of electron donors used by acidophilic prokaryotes ( )

Generic image for table
TABLE 1

Comparison of free energy changes associated with the oxidation of electron donors used by acidophilic prokaryotes ( )

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
/content/10.1128/9781555818821.ch4.3.1.ch4.3.1tab02
TABLE 2

Contrasting physiological properties of spp.

Generic image for table
TABLE 2

Contrasting physiological properties of spp.

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1
/content/10.1128/9781555818821.ch4.3.1.ch4.3.1tab03
TABLE 3

Physiological properties of acidophilic actinobacteria

Generic image for table
TABLE 3

Physiological properties of acidophilic actinobacteria

Citation: Barrie Johnson D, Aguilera A. 2016. The Microbiology of Extremely Acidic Environments, p 4.3.1-1-4.3.1-24. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.1

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