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Title: Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages

Journal Article · · Environmental Microbiology
 [1];  [1];  [1];  [2];  [3];  [3];  [4];  [5];  [1];  [6]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  2. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology; The Ohio State Univ., Columbus, OH (United States). School of Earth Sciences
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Geophysics, Division of Earth Sciences
  6. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy, and Management

Nitrogen, sulfur and carbon fluxes in the terrestrial subsurface are determined by the intersecting activities of microbial community members, yet the organisms responsible are largely unknown. Metagenomic methods can identify organisms and functions, but genome recovery is often precluded by data complexity. To address this limitation, we developed subsampling assembly methods to re-construct high-quality draft genomes from complex samples. We applied these methods to evaluate the interlinked roles of the most abundant organisms in biogeochemical cycling in the aquifer sediment. Community proteomics confirmed these activities. The eight most abundant organisms belong to novel lineages, and two represent phyla with no previously sequenced genome. Four organisms are predicted to fix carbon via the Calvin-Benson-Bassham, Wood-Ljungdahl or 3-hydroxyproprionate/4-hydroxybutarate pathways. The profiled organisms are involved in the network of denitrification, dissimilatory nitrate reduction to ammonia, ammonia oxidation and sulfate reduction/oxidation, and require substrates supplied by other community members. An ammonium-oxidizing Thaumarchaeote is the most abundant community member, despite low ammonium concentrations in the groundwater. This organism likely benefits from two other relatively abundant organisms capable of producing ammonium from nitrate, which is abundant in the groundwater. Overall, dominant members of the microbial community are interconnected through exchange of geochemical resources.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Natural Sciences and Engineering Research Council of Canada (NSERC); Work for Others (WFO)
Grant/Contract Number:
AC05-00OR22725; AC02-05CH11231
OSTI ID:
1328276
Alternate ID(s):
OSTI ID: 1470999
Journal Information:
Environmental Microbiology, Vol. 18, Issue 1; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 115 works
Citation information provided by
Web of Science

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Microbial diversity in Huguangyan Maar Lake of China revealed by high–throughput sequencing journal January 2019
Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system journal March 2016
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
A new view of the tree of life journal April 2016
Sporulation, bacterial cell envelopes and the origin of life journal June 2016
Peatland Acidobacteria with a dissimilatory sulfur metabolism journal February 2018
Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle journal February 2018
Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira journal March 2018
Diverse Marinimicrobia bacteria may mediate coupled biogeochemical cycles along eco-thermodynamic gradients journal November 2017
Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy journal May 2018
Targeted isolation and cultivation of uncultivated bacteria by reverse genomics journal September 2019
Building de novo reference genome assemblies of complex eukaryotic microorganisms from single nuclei journal January 2020
Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes journal January 2018
Microbial Communities of Low Temperature, Saline Groundwater Used for Therapeutical Purposes in North Poland journal January 2019
Distribution and activity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soil journal August 2016
Growth promotion and inhibition induced by interactions of groundwater bacteria journal August 2018
Iron- and aluminium-induced depletion of molybdenum in acidic environments impedes the nitrogen cycle: Mo depletion by Fe/Al precipitation at ORR journal November 2018
In situ meta‐omic insights into the community compositions and ecological roles of hadal microbes in the Mariana Trench journal August 2019
Nitrate- and nitrite-dependent anaerobic oxidation of methane: Nitrate/nitrite AOM journal November 2016
The life sulfuric: microbial ecology of sulfur cycling in marine sediments: Microbial sulfur cycling in marine sediments journal May 2017
IMP: a pipeline for reproducible reference-independent integrated metagenomic and metatranscriptomic analyses journal December 2016
Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems journal August 2018
Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi journal October 2018
Evidence for Microbial Mediated NO3− Cycling Within Floodplain Sediments During Groundwater Fluctuations journal July 2019
Stable and Variable Parts of Microbial Community in Siberian Deep Subsurface Thermal Aquifer System Revealed in a Long-Term Monitoring Study journal December 2016
Metagenomic Insights Into the Microbial Community and Nutrient Cycling in the Western Subarctic Pacific Ocean journal April 2018
Nitric Oxide Dismutase (nod) Genes as a Functional Marker for the Diversity and Phylogeny of Methane-Driven Oxygenic Denitrifiers journal July 2019
Ultradeep Microbial Communities at 4.4 km within Crystalline Bedrock: Implications for Habitability in a Planetary Context journal January 2020
Metagenomic analysis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone journal January 2016
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone journal January 2016
To Dereplicate or Not To Dereplicate? journal June 2020
Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance journal January 2020
Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi text January 2018
Metagenomic views of microbial dynamics influenced by hydrocarbon seepage in sediments of the Gulf of Mexico journal April 2020
Complete 4.55-Megabase-Pair Genome of “Candidatus Fluviicola riflensis,” Curated from Short-Read Metagenomic Sequences journal November 2017
A Small Effort for Researchers, a Big Gain for Soil Metaproteomics journal February 2020