skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

Journal Article · · The ISME Journal
 [1];  [2];  [1];  [2];  [2];  [2];  [3];  [2];  [4];  [2];  [4];  [5];  [5];  [6]
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. Univ. of Chicago, IL (United States)
  4. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
  5. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  6. Univ. of California, Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
+ Show Author Affiliations

Fermentation-based metabolism is an important ecosystem function often associated with environments rich in organic carbon, such as wetlands, sewage sludge and the mammalian gut. The diversity of microorganisms and pathways involved in carbon and hydrogen cycling in sediments and aquifers and the impacts of these processes on other biogeochemical cycles remain poorly understood. Here we used metagenomics and proteomics to characterize microbial communities sampled from an aquifer adjacent to the Colorado River at Rifle, CO, USA, and document interlinked microbial roles in geochemical cycling. The organic carbon content in the aquifer was elevated via acetate amendment of the groundwater occurring over 2 successive years. Samples were collected at three time points, with the objective of extensive genome recovery to enable metabolic reconstruction of the community. Fermentative community members include organisms from a new phylum, Melainabacteria, most closely related to Cyanobacteria, phylogenetically novel members of the Chloroflexi and Bacteroidales, as well as candidate phyla genomes (OD1, BD1-5, SR1, WWE3, ACD58, TM6, PER and OP11). These organisms have the capacity to produce hydrogen, acetate, formate, ethanol, butyrate and lactate, activities supported by proteomic data. The diversity and expression of hydrogenases suggests the importance of hydrogen metabolism in the subsurface. Our proteogenomic data further indicate the consumption of fermentation intermediates by Proteobacteria can be coupled to nitrate, sulfate and iron reduction. Thus, fermentation carried out by previously unknown members of sediment microbial communities may be an important driver of nitrogen, hydrogen, sulfur, carbon and iron cycling.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
DOE Contract Number:
AC02-05CH11231
OSTI ID:
1971631
Journal Information:
The ISME Journal, Vol. 8, Issue 7; ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English

References (54)

Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms journal September 2012
Prokaryotes: The unseen majority journal June 1998
High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment journal April 2012
Redox pathways in a petroleum contaminated shallow sandy aquifer: Iron and sulfate reductions journal July 2006
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization journal August 2012
Phylogenetic Distribution of Potential Cellulases in Bacteria journal December 2012
Bacterial Disproportionation of Elemental Sulfur Coupled to Chemical Reduction of Iron or Manganese journal January 1993
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla journal September 2012
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation journal October 2012
Dissimilatory Nitrite and Nitric Oxide Reductases journal January 1996
Isolation and characterization of autotrophic, hydrogen-utilizing, perchlorate-reducing bacteria journal September 2004
Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi journal June 2006
The genome of Geobacter bemidjiensis, exemplar for the subsurface clade of Geobacter species that predominate in Fe(III)-reducing subsurface environments. journal January 2010
Community-wide analysis of microbial genome sequence signatures journal January 2009
Distinct and diverse anaerobic bacterial communities in boreal lakes dominated by candidate division OD1 journal March 2012
A systematic investigation of multiheme c-type cytochromes in prokaryotes journal January 2010
Evidence for Direct Electron Transfer by a Gram-Positive Bacterium Isolated from a Microbial Fuel Cell journal September 2011
Review of mechanisms and quantification of priming effects journal October 2000
Analysis of Extensive [FeFe] Hydrogenase Gene Diversity Within the Gut Microbiota of Insects Representing Five Families of Dictyoptera journal September 2011
Characterization of a heme c nitrite reductase from a non-ammonifying microorganism, Desulfovibrio vulgaris Hildenborough journal August 2000
Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond journal April 2007
Metagenomic Evidence for H2 Oxidation and H2 Production by Serpentinite-Hosted Subsurface Microbial Communities journal January 2012
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla journal October 2013
Energy Conservation via Electron-Transferring Flavoprotein in Anaerobic Bacteria journal November 2007
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
Denitrifying Bacteria Isolated from Terrestrial Subsurface Sediments Exposed to Mixed-Waste Contamination journal March 2010
Development of a biomarker for Geobacter activity and strain composition; Proteogenomic analysis of the citrate synthase protein during bioremediation of U(VI): Geobacter citrate synthase biomarker journal December 2010
Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater journal June 2011
Induction of prophages from deep-subseafloor bacteria journal January 2011
Elemental Sulfur and Thiosulfate Disproportionation by Desulfocapsa sulfoexigens sp. nov., a New Anaerobic Bacterium Isolated from Marine Surface Sediment journal January 1998
Molecular Analysis of the Metabolic Rates of Discrete Subsurface Populations of Sulfate Reducers journal July 2011
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM journal January 2011
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling journal January 2013
Completed Genome Sequence of the Anaerobic Iron-Oxidizing Bacterium Acidovorax ebreus Strain TPSY journal March 2010
The Genome Sequence of the Obligately Chemolithoautotrophic, Facultatively Anaerobic Bacterium Thiobacillus denitrificans journal February 2006
The role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect journal November 2011
Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community journal November 2012
Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments journal July 2010
Nitrate attenuation in groundwater: A review of biogeochemical controlling processes journal October 2008
Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas journal June 2001
Oxidation of Reduced Inorganic Sulfur Compounds by Bacteria: Emergence of a Common Mechanism? journal July 2001
Nitrogenase gene diversity and microbial community structure: a cross-system comparison journal July 2003
Psychrophilic sulfate-reducing bacteria isolated from permanently cold Arctic marine sediments: description of Desulfofrigus oceanense gen. nov., sp. nov., Desulfofrigus fragile sp. nov., Desulfofaba gelida gen. nov., sp. nov., Desulfotalea psychrophila gen. nov., sp. nov. and Desulfotalea arctica sp. nov. journal October 1999
Hitherto Unknown [Fe-Fe]-Hydrogenase Gene Diversity in Anaerobes and Anoxic Enrichments from a Moderately Acidic Fen journal January 2010
The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production journal May 2009
Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction journal October 2006
The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria journal October 2013
Fluctuations in Species-Level Protein Expression Occur during Element and Nutrient Cycling in the Subsurface journal March 2013
Variably saturated flow and multicomponent biogeochemical reactive transport modeling of a uranium bioremediation field experiment journal November 2011
The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments journal September 2004
Timing the Onset of Sulfate Reduction over Multiple Subsurface Acetate Amendments by Measurement and Modeling of Sulfur Isotope Fractionation journal August 2012
Targeted Discovery of Glycoside Hydrolases from a Switchgrass-Adapted Compost Community journal January 2010
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment journal August 2013
DNA–DNA hybridization values and their relationship to whole-genome sequence similarities journal January 2007

Similar Records

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer
Journal Article · Tue Jul 08 00:00:00 EDT 2014 · The ISME Journal, 8(7):1452-1463 · OSTI ID:1971631
+11 more
Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla
Journal Article · Sat Feb 28 00:00:00 EST 2015 · Environmental Microbiology · OSTI ID:1971631
+1 more
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla
Journal Article · Tue Oct 22 00:00:00 EDT 2013 · mBio (Online) · OSTI ID:1971631
+7 more

Related Subjects

metagenomics
proteomics
candidate phylum
hydrogenase
fermentation
sulfate reduction
microbial diversity