Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments

Abstract

Geological sequestration in deep underground repositories is the prevailing proposed route for radioactive waste disposal. After the disposal of radioactive waste in the subsurface, H2 may be produced by corrosion of steel and, ultimately, radionuclides will be exposed to the surrounding environment. To evaluate the potential for microbial activities to impact disposal systems, we explored the microbial community structure and metabolic functions of a sediment-hosted ecosystem at the Horonobe Underground Research Laboratory, Hokkaido, Japan. Overall, we found that the ecosystem hosted organisms from diverse lineages, including many from the phyla that lack isolated representatives. The majority of organisms can metabolize H2, often via oxidative [NiFe] hydrogenases or electron-bifurcating [FeFe] hydrogenases that enable ferredoxin-based pathways, including the ion motive Rnf complex. Many organisms implicated in H2 metabolism are also predicted to catalyze carbon, nitrogen, iron and sulfur transformations. Notably, iron-based metabolism is predicted in a novel lineage of Actinobacteria and in a putative methane-oxidizing ANME-2d archaeon. We infer an ecological model that links microorganisms to sediment-derived resources and predict potential impacts of microbial activity on H2 consumption and retardation of radionuclide migration.

Geological degassing enhances microbial metabolism in the continental subsurface

“…Altiarchaeota can be divided into two clusters, Alti-1 and Alti-2, with the latter having a broader metabolic variability than Alti-1 14 . However, organisms of the Alti-1 cluster are those that can dominate entire ecosystems, as shown for multiple ecosystems across the globe 12,5,35,13 . We investigated the metabolic capacities of the newly recovered Altiarchaeum GA genome in comparison with other Altiarchaeota ( Fig.…”

“…We reconstructed genomes of previously unbinned metagenomes resulting in 785 newly assembled and classified bacteria (Table S3) representing 430 different organisms after dereplication. Combined with genomes and iRep results from previous studies 5,4,13 , we leveraged in situ replication measures of 907 bacteria (Table S5) spanning the vast majority of all known bacterial phyla (see Supplementary File S1). Interestingly, the average iRep value of bacteria of the individual ecosystems correlated negatively and highly significantly with sample depth when using all iRep values individually (p-value < 10 -4 ) and also when using the median per sampled ecosystem (p-value < 0.0031, Fig.…”

“…In other words, the deeper the origin of the retrieved sample, the lower the genome replication measure. 13 and CG 5 were used in this study after dereplication using dRep if not already performed on the available genomes.…”

“…Subsurface lithoautotrophic microbial communities 8 have been reported for many terrestrial ecosystems including the Fennoscandian shield 9 , the Columbia River basalt 8 , the Witwatersrand Basin 10 , and subsurface fluids discharged by Crystal Geyser 11 . While these subsurface ecosystems are usually dominated by bacteria, one exception are Altiarchaea, a genus the two phylogenetic clades of the phylum Altiarchaeota (also known as Alti-1) 12,5,13 . Alti-1 form biofilms using their characteristic nano-grappling hooks (hami) 14,15 .…”

Lateral gene transfer shapes the distribution of RuBisCO among Candidate Phyla Radiation bacteria and DPANN archaea

“…Major outstanding questions concern the full scale of RuBisCO diversity and how the various forms are distributed phylogenetically within the CPR and DPANN groups. Importantly, in the last few years, additional work has recovered CPR and DPANN genomes from a much wider array of environmental types, including additional groundwater locations, the deep subsurface, hydrocarbon-impacted environments, and the ocean [10][11][12] . Here, we examined over 300 genomes from metagenomes from these environments to further elucidate diversity, potential functions, and the evolutionary history of RuBisCO in members of the bacterial Candidate Phyla Radiation and DPANN archaea.…”