A Unique Intersection of Physicochemical Conditions Controls the Formation of Geothermal Iron Oxide Microbial Mats

Context regarding our current paper in Nature Microbiology focused on the Marsarchaeota.
Published in Microbiology
A Unique Intersection of Physicochemical Conditions Controls the Formation of Geothermal Iron Oxide Microbial Mats

The paper in Nature Microbiology is here: https://go.nature.com/2Gffh9b

The natural world reveals the fundamental underpinnings that have guided the evolution of life. When we first encountered the iron oxide microbial mats in Yellowstone National Park, nothing was known about the organisms responsible or the geochemical conditions necessary for their formation. The amazing series of terracettes (see video1) form in the temperature range ~ 60-80 oC in acidic geothermal outflow channels containing ferrous Fe (~ 25-100 µM Fe) that is oxidized by members of the Sulfolobales (Metallosphaera spp.). As these reduced fluids interact with oxygen, the microbial oxidation of ferrous Fe results in the deposition of Fe(III)-oxides whose crystallinities and composition vary with geochemical conditions. The intersection of hydrodynamic, geochemical and microbial conditions necessary for Marsarchaeota is unique to landscape positions located just down gradient of spring discharge where thin-films are oxygenated as they flow across terracettes comprised of Fe(III)-oxides and cells.

The collection of diverse archaea and bacteria that live in these mats are stratified across temperature and oxygen gradients and represent 6 to 7 major lineages of Archaea as well as an important member of the bacterial Aquificales (Hydrogenobaculum). Representatives of the Marsarchaeota described in our recent manuscript often comprise 20 to 50 percent of the Fe-mat microbial community across temperatures from ~ 60-80 oC. Two groups of the Marsarchaeota are found in numerous different Fe mats along with members of a sister lineage described previously as the Geoarchaeota2. Both occupy microaerobic habitats, are likely organotrophic, synthesize the cofactor F420, and contain numerous F420-dependent proteins. Marsarchaeota were noted in a prior study by Beam et al.3 to be secondary colonizers in Fe-mats and were more abundant in mat positions below a more oxygenated surface zone. Enrichment cultures with a majority of G2 Marsarchaeota were shown to reduce Fe(III)-oxides, although no definitive mechanism was identified for this biotic process.

The experiential component of our research on Fe(III)-oxide microbial mats dates to 1999-2000. Since this time, we have made numerous trips annually to monitor and/or sample Fe microbial mats. We have noticed that new visual observations and discussions occurred during every field trip. These cumulative insights ultimately lead to a comprehensive description of the assembly and succession of geothermal Fe(III)-oxide mats in YNP3 as well as results reported here on Marsarchaeota. The role of low oxygen in supporting micro-aerobic archaea that are basal to the Crenarchaeota suggest that the Marsarchaeota, along with members of the Geoarchaeota, Thaumarchaeota and Thermoplasmatales-like Euryarchaeota, were important in the evolution of aerobic respiration in the archaea. These chemotrophs may have been metabolizing oxygen at low levels prior to or during early periods of the Great Oxidation Event. The physiology observed in the modern-day microbial mats described here show that Marsarchaeota express high levels of heme copper oxidases necessary for aerobic respiration in environments containing very low oxygen. These findings may provide clues regarding the origin of aerobic respiration, and the role of high Fe habitats in the evolution of archaea. 

1 Video link (also on site): https://drive.google.com/file/d/1Eb5FJeu_FllDp-U7PBo_eDPK3edKcDZV/view?usp=sharing

2 Kozubal, M. A. et al. Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park. ISME J. 7, 622–634 (2013).

3Beam, J. P. et al. Assembly and succession of iron oxide microbial mat communities in acidic geothermal springs. Front. Microbiol. 25 (2016). doi:10.3389/fmicb.2016.00025

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