Novel Microbial Groups Drive Productivity in an Archean Iron Formation

Abstract

Deep subsurface environments are decoupled from Earth’s surface processes yet diverse, active, and abundant microbial communities thrive in these isolated environments. Microbes inhabiting the deep biosphere face unique challenges such as electron donor/acceptor limitations, pore space/fracture network limitations, and isolation from other microbes within the formation. Of the few systems that have been characterized, it is apparent that nutrient limitations likely facilitate diverse microbe-microbe interactions (i.e., syntrophic, symbiotic, or parasitic) and that these interactions drive biogeochemical cycling of major elements. Here we describe microbial communities living in low temperature, chemically reduced brines at the Soudan Underground Mine State Park, United States. The Soudan Iron mine intersects a massive hematite formation at the southern extent of the Canadian Shield. Fractured rock aquifer brines continuously flow from exploratory boreholes drilled circa 1960 and are enriched in deuterium compared to the global meteoric values, indicating brines have had little contact with surface derived waters, and continually degas low molecular weight hydrocarbons C1-C4. Microbial enrichments suggest that once brines exit the boreholes, oxidation of the hydrocarbons occur. Amplicon sequencing show these borehole communities are low in diversity and dominated by Firmicute and Proteobacteria phyla. From the metagenome assemblies, we recovered approximately thirty genomes with estimated completion over 50%. Analysis of genome taxonomy generally followed the amplicon data, and highlights that several of the genomes represent novel families and genera. Metabolic reconstruction shows two carbon-fixation pathways were dominant, the Wood-Ljungdahl (acetogenesis) and Calvin-Benson-Bassham (via RuBisCo), indicating that inorganic carbon likely enters into the microbial foodweb with differing carbon fractionation potentials. Interestingly, methanogenesis is likely driven by Methanolobus and suggests cycling of methylated compounds and not H2/CO2 or acetate. Furthermore, the abundance of sulfate in brines suggests cryptic sulfur cycling may occur, as we detect possible sulfate reducing and thiosulfate oxidizing microorganisms. Finally, a majority of the microorganisms identified contain genes that would allow them to participate in several element cycles, highlighting that in these deep isolated systems metabolic flexibility may be an important life history trait.

Characterization of Martelella soudanensis sp. nov., Isolated from a Mine Sediment

“…However, there were some differences in the respective compositions of some long-chain fatty acids, such as C18:1 ω5c, C19:0 iso, and C20:1 ω7c. The respiratory quinones of strains NC18 T and NC20 were Q-10, typical for the genus Martelella [ 1 , 2 , 3 , 4 , 5 , 6 ].…”

“…Data for strain 1 from this study. Data for strain 3 from Rivas et al [ 1 ], strains 4 and 8 from Chung et al [ 4 ], strain 5 from Bibi et al [ 2 ], strains 6 and 9 from Zhang et al [ 3 ], strain 7 from Kim et al [ 6 ], and strain 10 from Lee [ 5 ]. +, positive; -, negative; w, weak; NR, not reported.…”

“…Although deep subsurface environments are characterized by relatively low available organic carbon and elevated pressure, they are the largest habitats for prokaryotes, estimated to contain from 12% to 20% of the total biomass of microorganisms on Earth [ 1 , 2 ]. The deep biosphere contains a variety of functionally active microbial communities, but microbes face challenges such as limited available electron donors or acceptors, pore space, and fracture networks, and competition with other microorganisms for growth [ 3 ]. The Soudan Iron Mine is located in northern Minnesota, USA, along the southern edge of the Canadian Shield Transects and the Archaean Animikie ocean basin.…”

“…The Soudan Iron Mine is located in northern Minnesota, USA, along the southern edge of the Canadian Shield Transects and the Archaean Animikie ocean basin. The mine reaches a depth of 714 m below the surface, providing access to deep subsurface brines entrained in a massive hematite formation [ 3 , 4 ]. Previous cultivation-based and metagenomics studies reported the presence of diverse microbial communities, including the iron-oxidizing Marinobacter and iron-reducing Desulfuromonas in a calcium- and sodium-rich brine that reaches salinities as high as 4.2% ( w / v ) from these boreholes [ 3 , 5 , 6 ].…”

N2 in deep subsurface fracture fluids of the Canadian Shield: Source and possible recycling processes

“…Microbially-driven anaerobic oxidation of ammonium (e.g., Van De Graaf et al, 1995;Byrne et al, 2008) is a more efficient mechanism to convert ammonium to N2. Microbial recycling of nitrogen has been suggested to occur in subsurface fracture fluids in the Kaapvaal Craton (Silver et al, 2012;Lau et al 2016) and elsewhere in the Canadian Shield (Sheik et al, 2021), but cannot be explored further for the KC samples due to the lack of biogeochemical data and isotopic compositions of other nitrogen species (ammonium, nitrite or nitrate, if there is any) in these fracture fluids. It is worth highlighting though that recent studies using cell counts and culture-based methods have identified low abundance of H2-utilizing, alkane-oxidizing sulfate-reducing bacteria in the KC fracture fluids (Lollar et al, 2019;Wilpiszeski et al, 2020).…”