Epilithic Microbial Community Functionality in Deep Oligotrophic Continental Bedrock

Abstract

The deep terrestrial biosphere hosts vast sessile rock surface communities and biofilms, but thus far, mostly planktic communities have been studied. We enriched deep subsurface microbial communities on mica schist in microcosms containing bedrock groundwater from the depth of 500 m from Outokumpu, Finland. The biofilms were visualized using scanning electron microscopy, revealing numerous different microbial cell morphologies and attachment strategies on the mica schist surface, e.g., bacteria with outer membrane vesicle-like structures, hair-like extracellular extensions, and long tubular cell structures expanding over hundreds of micrometers over mica schist surfaces. Bacterial communities were analyzed with amplicon sequencing showing that Pseudomonas, Desulfosporosinus, Hydrogenophaga, and Brevundimonas genera dominated communities after 8–40 months of incubation. A total of 21 metagenome assembled genomes from sessile rock surface metagenomes identified genes involved in biofilm formation, as well as a wide variety of metabolic traits indicating a high degree of environmental adaptivity to oligotrophic environment and potential for shifting between multiple energy or carbon sources. In addition, we detected ubiquitous organic carbon oxidation and capacity for arsenate and selenate reduction within our rocky MAGs. Our results agree with the previously suggested interaction between the deep subsurface microbial communities and the rock surfaces, and that this interaction could be crucial for sustaining life in the harsh anoxic and oligotrophic deep subsurface of crystalline bedrock environment.

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

“…The majority (≥ 75%) of the high quality Chloro exota MAGs encoded marker genes involved in several processes previously associated with the Chloro exota (Table S7B), including fatty acid degradation [50,55], formate oxidation [56], aerobic CO oxidation [57] and selenate reduction [53]. Except for the Anaerolineales, over 66% of the MAGs in the other ve orders had the capacity for degradation of aromatic compounds, as previously reported for Chloro exi from the marine subsurface [51].…”

“…While the Patescibacteria likely rely on symbiotic or parasitic relationships, members of the Chloro exota phylum are diverse and metabolically exible organisms, capable of thriving in a wide variety of geochemical niches. Chloro exota are abundant and widely distributed in a variety of environments, including terrestrial soils, sediments and groundwater, freshwater, pelagic oceans, and the marine subsea oor and sediments [49][50][51][52][53][54][55], and hydrothermal settings such as Guaymas Basin [11] and Brothers submarine volcano [8]. Genomic evidence suggests that Chloro exota are associated with important metabolisms in the carbon cycle, including fermentation, carbon xation, acetogenesis and the utilization of sugars, polymers, fatty acids, organic acids and other organic carbon compounds [50,51,54].…”

Depth wide distribution and metabolic potential of chemolithoautotrophic microorganisms reactivated from deep continental granitic crust underneath the Deccan Traps at Koyna, India

“…Samples from different subsurface settings have been previously used to investigate the abundance, nature, and substrate specific response of deep dwelling organisms via several cultivation-based methods and enrichment studies ( Kotelnikova and Pedersen, 1998 ; Hallbeck and Pedersen, 2008 , 2012 ; Fichtel et al, 2015 ; Rajala et al, 2015 ; Russell et al, 2016 ; Purkamo et al, 2017 , 2020 ; Rajala and Bomberg, 2017 ; Leandro et al, 2018 ; Imachi et al, 2019 ; Sanz et al, 2021 ; Nuppunen-Puputti et al, 2022 ). The outcome of these studies, resulted in the enrichment of microorganisms mostly belonging to bacterial phyla Proteobacteria, Firmicutes, Actinobacteria, Chloroflexi and Bacteroidetes ( Rastogi et al, 2009 , 2013 ; Fichtel et al, 2012 ; Fortunato and Huber, 2016 ; Rajala and Bomberg, 2017 ; Leandro et al, 2018 ) and archaeal members including Euryarchaeota, Thaumarchaeota and Crenarchaeota ( Zeng et al, 2009 ; Nuppunen-Puputti et al, 2018 ; Imachi et al, 2020 ; Alain et al, 2021 ; Courtine et al, 2021 ; Li et al, 2021 ).…”

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

“…The majority (≥75%) of the high quality Chloroflexota MAGs encoded marker genes involved in several processes previously associated with the Chloroflexota (Table S7B), including fatty acid degradation [50, 55], formate oxidation [56], aerobic CO oxidation [57] and selenate reduction [53]. Except for the Anaerolineales, over 66% of the MAGs in the other five orders had the capacity for degradation of aromatic compounds, as previously reported for Chloroflexi from the marine subsurface [51].…”

“…For example, putative homologs of the PKD repeat containing protein (MBS8122536.1), a hypothetical protein While the Patescibacteria likely rely on symbiotic or parasitic relationships, members of the Chloroflexota phylum are diverse and metabolically flexible organisms, capable of thriving in a wide variety of geochemical niches. Chloroflexota are abundant and widely distributed in a variety of environments, including terrestrial soils, sediments and groundwater, freshwater, pelagic oceans, and the marine subseafloor and sediments [49][50][51][52][53][54][55], and hydrothermal settings such as Guaymas Basin [11] and Brothers submarine volcano [8]. Genomic evidence suggests that Chloroflexota are associated with important metabolisms in the carbon cycle, including fermentation, carbon fixation, acetogenesis and the utilization of sugars, polymers, fatty acids, organic acids and other organic carbon compounds [50,51,54].…”