DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Novel candidate taxa contribute to key metabolic processes in Fennoscandian Shield deep groundwaters

Journal Article · · ISME Communications
 [1];  [1];  [1];  [2];  [3];  [4];  [1];  [1];  [1];  [2];  [4];  [4]
  1. Linnaeus University, Kalmar (Sweden)
  2. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  3. Linnaeus University, Kalmar (Sweden); Swedish University of Agricultural Sciences, Uppsala (Sweden)
  4. Swedish University of Agricultural Sciences, Uppsala (Sweden)

The continental deep biosphere contains a vast reservoir of microorganisms, although a large proportion of its diversity remains both uncultured and undescribed. In this study, the metabolic potential (metagenomes) and activity (metatranscriptomes) of the microbial communities in Fennoscandian Shield deep subsurface groundwaters were characterized with a focus on novel taxa. DNA sequencing generated 1270 de-replicated metagenome-assembled genomes and single-amplified genomes, containing 7 novel classes, 34 orders, and 72 families. The majority of novel taxa were affiliated with Patescibacteria, whereas among novel archaea taxa, Thermoproteota and Nanoarchaeota representatives dominated. Metatranscriptomes revealed that 30 of the 112 novel taxa at the class, order, and family levels were active in at least one investigated groundwater sample, implying that novel taxa represent a partially active but hitherto uncharacterized deep biosphere component. The novel taxa genomes coded for carbon fixation predominantly via the Wood–Ljungdahl pathway, nitrogen fixation, sulfur plus hydrogen oxidation, and fermentative pathways, including acetogenesis. These metabolic processes contributed significantly to the total community’s capacity, with up to 9.9% of fermentation, 6.4% of the Wood–Ljungdahl pathway, 6.8% of sulfur plus 8.6% of hydrogen oxidation, and energy conservation via nitrate (4.4%) and sulfate (6.0%) reduction. Key novel taxa included the UBA9089 phylum, with representatives having a prominent role in carbon fixation, nitrate and sulfate reduction, and organic and inorganic electron donor oxidation. These data provided insights into deep biosphere microbial diversity and their contribution to nutrient and energy cycling in this ecosystem.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2472469
Journal Information:
ISME Communications, Journal Name: ISME Communications Journal Issue: 1 Vol. 4; ISSN 2730-6151
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (90)

Äspö, SE Sweden: a natural groundwater flow model derived from hydrogeochemical observations journal November 1995
Methylomonas scandinavica sp.nov., a New Methanotrophic Psychrotrophic Bacterium isolated from Deep Igneous Rock Ground Water of Sweden journal December 1999
Characterization of microbial processes in deep aquifers of the Fennoscandian Shield journal July 2008
Understanding groundwater chemistry using mixing models journal July 2008
Genetic manipulation of Patescibacteria provides mechanistic insights into microbial dark matter and the epibiotic lifestyle journal October 2023
Metabolic versatility in methanogens journal October 2014
Anaerobic microbial manganese oxidation and reduction: A critical review journal May 2022
Effect of Tunnel Excavation on Source and Mixing of Groundwater in a Coastal Granitoidic Fracture Network journal November 2012
A hydrogen-based subsurface microbial community dominated by methanogens journal January 2002
A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust journal September 2015
Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations journal October 2015
Connectivity to the surface determines diversity patterns in subsurface aquifers of the Fennoscandian shield journal March 2016
Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments journal March 2017
Energy and carbon metabolisms in a deep terrestrial subsurface fluid microbial community journal June 2017
Insights into the phylogeny and coding potential of microbial dark matter journal July 2013
Complex archaea that bridge the gap between prokaryotes and eukaryotes journal May 2015
Unusual biology across a group comprising more than 15% of domain Bacteria journal June 2015
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Diverse uncultivated ultra-small bacterial cells in groundwater journal February 2015
A new view of the tree of life journal April 2016
Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria journal November 2014
Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle journal February 2018
An archaeal symbiont-host association from the deep terrestrial subsurface journal May 2019
Active sulfur cycling in the terrestrial deep subsurface journal February 2020
Groundwater Elusimicrobia are metabolically diverse compared to gut microbiome Elusimicrobia and some have a novel nitrogenase paralog journal July 2020
Prokaryotic taxonomy and nomenclature in the age of big sequence data journal April 2021
Candidatus Eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations journal March 2021
Large-scale protein level comparison of Deltaproteobacteria reveals cohesive metabolic groups journal July 2021
Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface journal February 2022
Connecting structure to function with the recovery of over 1000 high-quality metagenome-assembled genomes from activated sludge using long-read sequencing journal March 2021
Energy efficiency and biological interactions define the core microbiome of deep oligotrophic groundwater journal July 2021
Lytic archaeal viruses infect abundant primary producers in Earth’s crust journal July 2021
Terrigenous dissolved organic matter persists in the energy-limited deep groundwaters of the Fennoscandian Shield journal August 2022
Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments journal August 2022
Thiobacillus as a key player for biofilm formation in oligotrophic groundwaters of the Fennoscandian Shield journal June 2023
Carbon fixation rates in groundwater similar to those in oligotrophic marine systems journal June 2022
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life journal September 2017
Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface journal January 2018
Expanding anaerobic alkane metabolism in the domain of Archaea journal March 2019
An archaeal origin of the Wood–Ljungdahl H4MPT branch and the emergence of bacterial methylotrophy journal August 2019
SeqCode: a nomenclatural code for prokaryotes described from sequence data journal September 2022
Hyperactive nanobacteria with host-dependent traits pervade Omnitrophota journal March 2023
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations journal September 2018
The Fennoscandian Shield deep terrestrial virosphere suggests slow motion ‘boom and burst’ cycles journal March 2021
Connectivity of Fennoscandian Shield terrestrial deep biosphere microbiomes with surface communities journal January 2022
Ultra-small bacteria and archaea exhibit genetic flexibility towards groundwater oxygen content, and adaptations for attached or planktonic lifestyles journal February 2023
HydDB: A web tool for hydrogenase classification and analysis journal September 2016
An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers journal November 2016
Viable cyanobacteria in the deep continental subsurface journal October 2018
Structural and Chemical Characterization of a Natural Fracture Surface from 2.8 Kilometers Below Land Surface: Biofilms in the Deep Subsurface journal September 2006
GTDB-Tk v2: memory friendly classification with the genome taxonomy database journal October 2022
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
Investigation of viable taxa in the deep terrestrial biosphere suggests high rates of nutrient recycling journal June 2018
Global diversity and inferred ecophysiology of microorganisms with the potential for dissimilatory sulfate/sulfite reduction journal September 2023
Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations journal May 2015
High diversity, abundance, and expression of hydrogenases in groundwater journal January 2024
Microbial ecology of the deep terrestrial subsurface journal January 2024
mOTUpan: a robust Bayesian approach to leverage metagenome-assembled genomes for core-genome estimation journal July 2022
Note: Desulfovibrio aespoeensis sp. nov., a mesophilic sulfate-reducing bacterium from deep groundwater at aspo hard rock laboratory, Sweden journal January 1998
A global perspective on bacterial diversity in the terrestrial deep subsurface journal January 2023
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Sub‐seafloor biogeochemical processes and microbial life in the Baltic Sea journal February 2020
Genomic characterization of three novel Desulfobacterota classes expand the metabolic and phylogenetic diversity of the phylum journal June 2021
A metagenomic view of novel microbial and metabolic diversity found within the deep terrestrial biosphere at DeMMO: A microbial observatory in South Dakota, USA journal November 2023
Subterranean microbial populations metabolize hydrogen and acetate under in situ conditions in granitic groundwater at 450 m depth in the Äspö Hard Rock Laboratory, Sweden journal April 2012
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic journal March 2009
Genomic signatures and co‐occurrence patterns of the ultra‐small Saccharimonadia (phylum CPR/Patescibacteria) suggest a symbiotic lifestyle journal September 2019
Taxonomic and carbon metabolic diversification of Bathyarchaeia during its coevolution history with early Earth surface environment journal July 2023
Environmental Genomics Reveals a Single-Species Ecosystem Deep Within Earth journal October 2008
Genomes of Novel Myxococcota Reveal Severely Curtailed Machineries for Predation and Cellular Differentiation journal November 2021
Ecological Aspects of the Distribution of Different Autotrophic CO 2 Fixation Pathways journal January 2011
The Ultramicrobacterium "Elusimicrobium minutum" gen. nov., sp. nov., the First Cultivated Representative of the Termite Group 1 Phylum journal March 2009
"Endomicrobia": Cytoplasmic Symbionts of Termite Gut Protozoa Form a Separate Phylum of Prokaryotes journal March 2005
Function of Periplasmic Hydrogenases in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough journal June 2007
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla journal October 2013
Statistical Analysis of Community RNA Transcripts between Organic Carbon and Geogas-Fed Continental Deep Biosphere Groundwaters journal August 2019
Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere journal November 2018
Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes journal September 2018
Measurement of in Situ Activities of Nonphotosynthetic Microorganisms in Aquatic and Terrestrial Habitats journal October 1985
Potential for hydrogen-oxidizing chemolithoautotrophic and diazotrophic populations to initiate biofilm formation in oligotrophic, deep terrestrial subsurface waters journal March 2017
METABOLIC: high-throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community-scale functional networks journal February 2022
The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers journal December 2021
Enzymology of the Wood-Ljungdahl Pathway of Acetogenesis journal March 2008
Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater journal September 2018
Depth and Dissolved Organic Carbon Shape Microbial Communities in Surface Influenced but Not Ancient Saline Terrestrial Aquifers journal November 2018
Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions journal June 2019
FeGenie: A Comprehensive Tool for the Identification of Iron Genes and Iron Gene Neighborhoods in Genome and Metagenome Assemblies journal January 2020
Rock Surface Fungi in Deep Continental Biosphere—Exploration of Microbial Community Formation with Subsurface In Situ Biofilm Trap journal December 2020
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies journal January 2019