Rare Biosphere Archaea Assimilate Acetate in Precambrian Terrestrial Subsurface at 2.2 km Depth

Abstract

The deep biosphere contains a large portion of the total microbial communities on Earth, but little is known about the carbon sources that support deep life. In this study, we used Stable Isotope Probing (SIP) and high throughput amplicon sequencing to identify the acetate assimilating microbial communities at 2260 m depth in the bedrock of Outokumpu, Finland. The long-term and short-term effects of acetate on the microbial communities were assessed by DNA-targeted SIP and RNA targeted cell activation. The microbial communities reacted within hours to the amended acetate. Archaeal taxa representing the rare biosphere at 2260 m depth were identified and linked to the cycling of acetate, and were shown to have an impact on the functions and activity of the microbial communities in general through small key carbon compounds. The major archaeal lineages identified to assimilate acetate and metabolites derived from the labelled acetate were Methanosarcina spp., Methanococcus spp., Methanolobus spp., and unclassified Methanosarcinaceae. These archaea have previously been detected in the Outokumpu deep subsurface as minor groups. Nevertheless, their involvement in the assimilation of acetate and secretion of metabolites derived from acetate indicated an important role in the supporting of the whole community in the deep subsurface, where carbon sources are limited.Geosciences 2018, 8, 418 2 of 20 utilizing soluble gases, such as crustal methane or hydrogen from radiolytic decomposition of water, have been made since [5][6][7][8]. More specifically, the metabolic capabilities of deep terrestrial subsurface microbial communities include the pathways covering, e.g., methanogenesis [9][10][11], anaerobic methane oxidation [12], acetogenesis [4,13], sulfate reduction [14-16], oxidation of sulfur by denitrification [17], and reduction of iron [14].The Outokumpu deep scientific drill hole, located in Eastern Finland, hosts a unique environment piercing through crystalline Precambrian bedrock and its numerous saline fluid filled fracture zones. The composition of the microbial communities and the geochemical characteristics of the Outokumpu deep subsurface have been studied in detail [11,[18][19][20][21][22][23][24][25][26][27]. The metabolic strategies of the microbial communities at different depths in Outokumpu have been estimated through functional gene analysis and metagenomes [11,21]. Purkamo et al. [21,22] suggested that microbial communities commonly employ heterotrophic carbon assimilation in the Outokumpu deep subsurface, and that the communities have the capacity of both sulphate and nitrate reduction. At greater depths, genetic potential for autotrophic acetogenesis and hydrogenotrophic methanogenesis has been detected from Outokumpu metagenomes together with H 2 oxidation and CO 2 fixation coupling hydrogenases [11].The terrestrial deep subsurface represents an oligotrophic, nutrient-poor, and isolated habitat. The fact that heterotrophy appears to be common in the Outokumpu deep biosphere means that the carbon sub...

Rock Surface Fungi in Deep Continental Biosphere—Exploration of Microbial Community Formation with Subsurface In Situ Biofilm Trap

“…They have been shown to produce nitrous oxide (N 2 O), and host Burkholderia -related endosymbiotic bacteria [ 89 ]. Various types of Burkholderia are common in Outokumpu groundwater, especially in the deeper part of the bedrock [ 50 , 58 ]. Both fungi and Burkholderia could have an advantage due to endosymbiotic relationships, which could help them to adapt to deep subsurface conditions.…”

“…For example, acetate is a carbon source for the microorganisms e.g., the chemolithotrophic Dethiobacter [ 96 ]. Similarly, the Outokumpu deep subsurface microbial communities have been shown to use acetate and benefit from acetate during enrichment [ 58 , 61 ]. Here, we showed that Dethiobacter attached to mica schist surfaces especially at 967 m depth.…”

“…The Outokumpu Deep Drill Hole is part of the International Continental Scientific Drilling Program (ICDP) infrastructure, . Previous studies have described the site and its hydrogeochemical characteristics [ 46 , 47 , 54 , 55 , 56 , 57 ], and microbial community structure and functionality in the fracture fluids [ 35 , 48 , 49 , 51 , 58 , 59 ]. The lithological profile of the Outokumpu Deep Drill Hole has been previously described and mica schist is the prevalent rock type at our incubation depths [ 53 , 60 ].…”

Ultradeep Microbial Communities at 4.4 km within Crystalline Bedrock: Implications for Habitability in a Planetary Context

“…The rare biosphere, i.e., OTUs comprising less than 1% of the total microbial community, was present in significant extent in both study sites. The rare biosphere represents an important gene pool and may in fact play a disproportionately large role in biogeochemical cycling [92,93]. Interestingly, we could also detect some archaea that usually represent a minor part of the total community in deep subsurface environments, and some fungal signals as well.…”

Biogeography, Assembly Patterns, Driving Factors, and Interactions of Archaeal Community in Mangrove Sediments

“…Hence, the microbes of the “rare biosphere” have important roles in the metabolic and ecological functions of aquatic habitats ( 26 – 28 ). For example, rare archaea are supposed to have ecological functions, such as acetate metabolism ( 29 ), carbon cycling ( 30 ), and methanogenesis ( 31 ). Another interesting component is the taxa which are usually rare but occasionally become more prominent under optimal conditions, namely, the conditionally rare taxa ( 26 , 28 , 32 ).…”