Epilithic Microbial Community Functionality in Deep Oligotrophic Continental Bedrock.

Maija Nuppunen-Puputti,Malin Bomberg,Aino Soro,Lotta Purkamo,Ilmo Kukkonen,Riikka Kietäväinen,Mari Raulio

doi:10.3389/fmicb.2022.826048

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.

Highlights

Deep life in continental bedrock inhabits both groundwater and all water-covered rock surfaces and fractures
Hyphaelike cell tubings expanded over tens to hundreds of micrometers across the mica schist surfaces (Supplementary Figures 1A,B)
metagenome assembled genomes (MAGs) affiliating with major mica schist microbial community groups would potentially specialize in sulfur cycling, whereas minor group representing MAGs had genetic potential for a fermentative lifestyle, and for carbon monoxide, arsenate, and selenate cycling

Summary

Introduction

Deep life in continental bedrock inhabits both groundwater and all water-covered rock surfaces and fractures. Microbes attach to rock surfaces, remaining as single sessile cells or forming microcolonies and biofilms (Wanger et al, 2006; Escudero et al, 2018). Deep continental microbial biomass has been estimated to constitute up to 19% of the Earth’s biomass (McMahon and Parnell, 2014; Bar-On et al, 2018; Magnabosco et al, 2018). 20–80% of the deep subsurface microbial biomass resides in biofilms (Flemming and Wuertz, 2019), which means that the previous biomass evaluations may be underestimated. Challenges related to difficulty of retrieving native deep subsurface biofilm samples and how biofilm are defined for these calculations remain (Bar-On and Milo, 2019; Flemming and Wuertz, 2019). Dense biofilms in deep anaerobic biosphere may not form and all mineral attached single cells are considered as biofilm in these estimations (Moser et al, 2003; Wanger et al, 2006; Magnabosco et al, 2018; Flemming and Wuertz, 2019). Microbial cell abundance in crushed deep rock core from the Deccan traps, India, have been shown to reach nearly 105 cells per gram estimated by qPCR (Dutta et al, 2018)

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Conclusion