Archaeal Communities in Deep Terrestrial Subsurface Underneath the Deccan Traps, India

Abstract

Archaeal community structure and potential functions within the deep, aphotic, oligotrophic, hot, igneous provinces of ∼65 Myr old basalt and its Archean granitic basement was explored through archaeal 16S rRNA gene amplicon sequencing from extracted environmental DNA of rocks. Rock core samples from three distinct horizons, basaltic (BS), transition (weathered granites) (TZ) and granitic (GR) showed limited organic carbon (4–48 mg/kg) and varied concentrations (<1.0–5000 mg/kg) of sulfate, nitrate, nitrite, iron and metal oxides. Quantitative PCR estimated the presence of nearly 10 3 –10 4 archaeal cells per gram of rock. Archaeal communities within BS and GR horizons were distinct. The absence of any common OTU across the samples indicated restricted dispersal of archaeal cells. Younger, relatively organic carbon- and Fe 2 O 3 -rich BS rocks harbor Euryarchaeota , along with varied proportions of Thaumarchaeota and Crenarchaeota . Extreme acid loving, thermotolerant sulfur respiring Thermoplasmataceae , heterotrophic, ferrous-/H-sulfide oxidizing Ferroplasmaceae and Halobacteriaceae were more abundant and closely interrelated within BS rocks. Samples from the GR horizon represent a unique composition with higher proportions of Thaumarchaeota and uneven distribution of Euryarchaeota and Bathyarchaeota affiliated to Methanomicrobia , SAGMCG-1, FHMa11 terrestrial group, AK59 and unclassified taxa. Acetoclastic methanogenic Methanomicrobia , autotrophic SAGMCG-1 and MCG of Thaumarcheaota could be identified as the signature groups within the organic carbon lean GR horizon. Sulfur-oxidizing Sulfolobaceae was relatively more abundant in sulfate-rich amygdaloidal basalt and migmatitic gneiss samples. Methane-oxidizing ANME-3 populations were found to be ubiquitous, but their abundance varied greatly between the analyzed samples. Changes in diversity pattern among the BS and GR horizons highlighted the significance of local rock geochemistry, particularly the availability of organic carbon, Fe 2 O 3 and other nutrients as well as physical constraints (temperature and pressure) in a niche-specific colonization of extremophilic archaeal communities. The study provided the first deep sequencing-based illustration of an intricate association between diverse extremophilic groups (acidophile-halophile-methanogenic), capable of sulfur/iron/methane metabolism and thus shed new light on their potential role in biogeochemical cycles and energy flow in deep biosphere hosted by hot, oligotrophic igneous crust.

Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane

“…The 16S rRNA gene phylogeny ( Supplementary Figure S1a ) demonstrates that this microorganism is closely related to ANME-3 archaea detected in Haakon Mosby mud volcano, deep-sea sediments of Monterey Canyon, and some other habitats [ 3 , 4 , 79 ]. The mcrA gene of KA19 ( Supplementary Figure S1b ) phylogenetically belongs to «group f» cluster previously found to be associated with ANME-3 microorganisms [ 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 ,...…”

“…ANME-3 has been found mainly in marine ecosystems, including submarine mud volcanoes, deep-marine seeps, shallow and coastal sediments [ 3 , 6 , 7 , 26 , 34 , 35 , 36 , 37 ]. There is a single study report on the detection of ANME-3 in basaltic and granitic rock samples from the deep terrestrial subsurface [ 38 ]. The electron acceptors that ANME-3 utilize during AOM are unknown.…”

Identification and Metabolism of Naturally Prevailing Microorganisms in Zinc and Copper Mineral Processing

“…Some of those identified to the genus or class level and previously also found in mineral environments include for example, uncultured Thermoplasmatota group BSLdp215 that was found especially from ETAM Water and Ferroplasma from the Zn Rougher Feed. The group BSLdp215 has been found earlier in acidic iron-rich water from depths of 500 and 600 m from the Pyhäsalmi mine in Finland [77] and in deep, hot, basaltic rocks in India [78]; however, its role is unknown. Ferroplasma, on the other hand, are mesophilic, acidophilic and able to oxidize iron, pyrite and other metal sulfides; and they are often found in acid mine drainage environments and ore deposits and mines [79].…”

High Abundance of Thaumarchaeota Found in Deep Metamorphic Subsurface in Eastern China

“…To construct a phylogenetic tree of Thaumarchaeota sequences from this study, other thaumarchaeotal 16S rRNA gene sequences from the deep subsurface were also retrieved from the NCBI database. These sequence sources included fissure water and mine service water from gold mines in South Africa, with depths ranging from 0.7 to 3.08 km [ 27 ]; igneous rock from a borehole drilling project in the Deccan Traps in India, with depths ranging from ~60 to ~1400 m [ 26 ]; and metamorphic rocks from the CCSD borehole drilling project in eastern China [ 28 , 39 ]. The sequences from the Deccan Traps subsurface rock samples were produced by Illumina MiSeq sequencing, and the representative Thaumarchaeota sequences were obtained with DADA2 algorithm [ 36 ].…”

“…In some marine areas with low respiration, O 2 penetrates to a great depth in sediments and rocks [ 24 , 25 ], which allows for the presence of aerobic microorganisms, including Thaumarchaeota, in the marine deep subsurface. High abundances of Thaumarchaeota have also been found in deep terrestrial subsurface—including interior rock samples of the Deccan Traps, India, from depths of less than 100 m to as much as 1400 m [ 26 ]; and fissure waters from gold mines in South Africa at depths of up to 3.08 km [ 27 ]. In 2005, high abundances of archaea, which were mainly assigned to Crenarchaeota, were reported in metamorphic rock samples with depth of great than 2000 m from the Chinese Continental Scientific Drilling Project (CCSD) in eastern China [ 28 ], and most of the crenarchaeotal lineages were proved to be Thaumarchaeota in that study.…”