Abstract

Geochemical, molecular, and physiological analyses of microbial isolates were combined to study the geomicrobiology of acidic iron oxide mats in Yellowstone National Park. Nineteen sampling locations from 11 geothermal springs were studied ranging in temperature from 53 to 88°C and pH 2.4 to 3.6. All iron oxide mats exhibited high diversity of crenarchaeal sequences from the Sulfolobales, Thermoproteales, and Desulfurococcales. The predominant Sulfolobales sequences were highly similar to Metallosphaera yellowstonensis str. MK1, previously isolated from one of these sites. Other groups of archaea were consistently associated with different types of iron oxide mats, including undescribed members of the phyla Thaumarchaeota and Euryarchaeota. Bacterial sequences were dominated by relatives of Hydrogenobaculum spp. above 65–70°C, but increased in diversity below 60°C. Cultivation of relevant iron-oxidizing and iron-reducing microbial isolates included Sulfolobus str. MK3, Sulfobacillus str. MK2, Acidicaldus str. MK6, and a new candidate genus in the Sulfolobales referred to as Sulfolobales str. MK5. Strains MK3 and MK5 are capable of oxidizing ferrous iron autotrophically, while strain MK2 oxidizes iron mixotrophically. Similar rates of iron oxidation were measured for M. yellowstonensis str. MK1 and Sulfolobales str. MK5. Biomineralized phases of ferric iron varied among cultures and field sites, and included ferric oxyhydroxides, K-jarosite, goethite, hematite, and scorodite depending on geochemical conditions. Strains MK5 and MK6 are capable of reducing ferric iron under anaerobic conditions with complex carbon sources. The combination of geochemical and molecular data as well as physiological observations of isolates suggests that the community structure of acidic Fe mats is linked with Fe cycling across temperatures ranging from 53 to 88°C.

Highlights

  • Ferric iron oxyhydroxide and jarositic microbial mats are found in numerous environments and have been well studied in acid-minedrainage systems such as Iron Mountain, CA, USA (Edwards et al, 1999; Singer et al, 2008) where Fe(II) and H2SO4 are produced during the oxidation of sulfide minerals such as pyrite and chalcopyrite (Nordstrom and Southam, 1997; Rohwerder et al, 2003)

  • The Sulfolobales are important in all 18 spring www.frontiersin.org sites as indicated by the high percentage of 16S rRNA sequences and binning of metagenome sequence reads

  • Metagenome data strongly suggest that M. yellowstonensis-like populations are important in Norris Geyser Basin (NGB)-BE and NGB-OSP Springs as evidenced by the number of total reads binning to the M. yellowstonensis genome (Inskeep et al, 2010)

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Summary

Introduction

Ferric iron oxyhydroxide and jarositic microbial mats are found in numerous environments and have been well studied in acid-minedrainage systems such as Iron Mountain, CA, USA (Edwards et al, 1999; Singer et al, 2008) where Fe(II) and H2SO4 are produced during the oxidation of sulfide minerals such as pyrite and chalcopyrite (Nordstrom and Southam, 1997; Rohwerder et al, 2003). Ferric iron mats from acidic geothermal springs in Yellowstone National Park (YNP) provide an outstanding natural laboratory to study thermophilic microorganisms that utilize ferrous iron for energy acquisition coupled to CO2 fixation as their primary carbon source. Their ability to thrive in high-temperature environments with minimal requirements other than CO2 and inorganic constituents suggests that these organisms are important primary producers in acidic high-temperature environments. The limited energy available from the oxidation of Fe(II) results in the formation of copious amounts of iron oxides. Low cell numbers can result in the oxidation of large amounts of iron, www.frontiersin.org

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