Chapter 4.3.4 : Life in High-Temperature Environments

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A variety of thermal systems exist on Earth, spanning wide ranges of temperature and other physicochemical parameters, including the deep continental and marine subsurface, terrestrial and marine geothermal systems at tectonic plate boundaries, spreading centers, and "hotspots", and a wide variety of natural and engineered systems. A variety of hyperthermophilic and thermophilic microorganisms inhabit many of these environments; however, microbial diversity is inversely proportional to temperature at temperatures inhabited by thermophiles. Above ~80 {degree sign}C, microbial communities are almost entirely composed of thermophilic specialists, including Archaea such as Thermoprotei (Crenarchaeota), Archaeoglobi (Euryarchaeota), Methanopyri (Euryarchaeota), Thermococci (Euryarchaeota); Bacteria such as Aquificae, Thermi, Thermotogae, Thermodesulfobacteria, and Dictyoglomi; and a variety of yet-uncultivated lineages that are abundant globally. The decrease in diversity and change in microbial community composition associated with high temperatures is driven by bioenergetic stresses associated with increased degradation and racemization rates at high temperature. One key molecular adaptation to life at high temperature is the tetraether membrane lipid. Biodiversity losses driven by high temperature lead to losses in ecosystem functions that impact key biochemical processes, such as the absence of photosynthesis above ~73 {degree sign}C. The impact of high temperature on other biogeochemical cycles is still poorly understood, but likely includes limitations on the oxidative nitrogen cycle. A significant recent advancement of the study of life at high temperature is the use of single-cell genomics and metagenomics approaches to probe yet-uncultivated lineages in high-temperature habitats; however, this progress must be matched with an equally vigorous program to test functions predicted from these genomes.

Citation: Hedlund B, Thomas S, Dodsworth J, Zhang C, Miller R. 2016. Life in High-Temperature Environments, p 4.3.4-1-4.3.4-15. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.4
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Image of FIGURE 1

Generalized schematic of terrestrial geothermal systems such as those in Yellowstone National Park. Local or regional aquifers sourced by meteoric water follow fault lines or permeable layers and become heated by proximity to shallow magma bodies or heated rocks. Heated water may boil in the subsurface due to adiabatic decompression as fluids rise. Dissolved gases such as H, HS, and NH become enriched in vapor phases, which source either fumaroles (a) or acidic pools or mudpots (b). These so-called vapor-dominated systems become acidified to pH 1.5–3.5 by biotic and abiotic oxidation of HS to sulfuric acid at or near the surface; acid weathers the host rock and solubilizes clays. The liquid phase, typically with lower concentrations of volatiles, but enriched in soluble ions such as Na and Cl, is buffered to pH 7–9 by the carbonate buffering system and may source large, clear pools or streams with substantial discharge (c). doi:10.1128/9781555818821.ch4.3.4.f1

Citation: Hedlund B, Thomas S, Dodsworth J, Zhang C, Miller R. 2016. Life in High-Temperature Environments, p 4.3.4-1-4.3.4-15. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.4
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Image of FIGURE 2

Terrestrial geothermal systems at a variety of scales. (a–c) Abundant microbial growth in Octopus Spring, a high-temperature, alkaline spring in Yellowstone National Park's Lower Geyser Basin. (a) View of the source pool (∼92°C; pH ∼ 8.0) from above the “head” of the Octopus, with outflow streams (“tentacles”) flowing away and to the right (arrow, site of pink streamer community). (b) Pink streamer community in the outflow of Octopus Spring at ∼84 to 88°C, with abundant growth of and yet-uncultivated lineages ( ) (width of view, ∼0.3 m). (c) Scanning electron micrograph (SEM) of a pure culture of isolated from Octopus Spring showing flow-dependent filamentous morphology (bar, 2 µm; used with permission from [ ]). (d–f) Sharp transition of phototrophic biofilm growth in Mud Hot Spring (Sandy's Spring West) in the U.S. Great Basin. (d) View of the source pool (∼86°C; pH ∼ 7.2) with the upper temperature limit of photosynthesis clearly visible (arrow, ∼73°C). (e) Close up of the outflow channel showing the upper temperature limit of photosynthesis (arrow; width of view, ∼0.5 m). (f) SEM of a pure culture of , an abundant resident of sediments in Mud Hot Spring and nearby Great Boiling Spring ( ) (bar, arrow, ∼2 µm; arrows, septa between individual cells in filaments). (g–i) Diretiyanqu (“Experimental Site”), an acidic system in Tengchong, China, and abundant microorganisms. (g) Large, geothermally altered erosional feature typical of many acidic geothermal systems (arrow, area in focus in H). (h) One of several hot, acidic pools (∼86°C; pH ∼ 2.6) actively gassing and with thermoacidophilic algae () visible in vapor condensate (arrow; width of view, ∼0.5 m). (i) Transmission electron micrograph of , the dominant microorganism at this site ( ) with spindle-shaped virus (STSV1) (arrow; bar, 1 µm; used with permission from [ ]). doi:10.1128/9781555818821.ch4.3.4.f2

Citation: Hedlund B, Thomas S, Dodsworth J, Zhang C, Miller R. 2016. Life in High-Temperature Environments, p 4.3.4-1-4.3.4-15. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.4
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Image of FIGURE 3

Example core tetraether lipid structures. (a) Example isoprenoid dialkyl glycerol tetraethers (iGDGTs) found in thermophilic and ; increasing cyclization is associated with increased temperature and/or decreased pH (top to bottom). (b) Thaumarchaeol (formerly crenarchaeol), a distinctive lipid of both thermophilic and mesophilic . (c) Example branched GDGTs (bGDGTs) produced by mesophilic and likely produced by unknown moderate thermophiles; methylation is inversely proportional to temperature in terrestrial geothermal systems. Figure modified from ( ). doi:10.1128/9781555818821.ch4.3.4.f3

Citation: Hedlund B, Thomas S, Dodsworth J, Zhang C, Miller R. 2016. Life in High-Temperature Environments, p 4.3.4-1-4.3.4-15. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch4.3.4
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