Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer
Abstract
Groundwater ecosystems are conventionally thought to be fueled by surface-derived allochthonous organic matter and dominated by heterotrophic microbes living under often-oligotrophic conditions. However, in a 2-month study of nitrate amendment to a perennially suboxic aquifer in Rifle (CO), strain-resolved metatranscriptomic analysis revealed pervasive and diverse chemolithoautotrophic bacterial activity relevant to C, S, N and Fe cycling. Before nitrate injection, anaerobic ammonia-oxidizing (anammox) bacteria accounted for 16% of overall microbial community gene expression, whereas during the nitrate injection, two other groups of chemolithoautotrophic bacteria collectively accounted for 80% of the metatranscriptome: (1) members of the Fe(II)-oxidizing Gallionellaceae family and (2) strains of the S-oxidizing species, Sulfurimonas denitrificans. Notably, the proportion of the metatranscriptome accounted for by these three groups was considerably greater than the proportion of the metagenome coverage that they represented. Transcriptional analysis revealed some unexpected metabolic couplings, in particular, putative nitrate-dependent Fe(II) and S oxidation among nominally microaerophilic Gallionellaceae strains, including expression of periplasmic (NapAB) and membrane-bound (NarGHI) nitrate reductases. The three most active groups of chemolithoautotrophic bacteria in this study had overlapping metabolisms that allowed them to occupy different yet related metabolic niches throughout the study. Overall, these results highlight the important role that chemolithoautotrophy can have inmore »
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States)
- OSTI Identifier:
- 1377452
- Grant/Contract Number:
- AC02-05CH11231; S10RR029668; S10RR027303
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 9; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES
Citation Formats
Jewell, Talia N. M., Karaoz, Ulas, Brodie, Eoin L., Williams, Kenneth H., and Beller, Harry R. Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer. United States: N. p., 2016.
Web. doi:10.1038/ismej.2016.25.
Jewell, Talia N. M., Karaoz, Ulas, Brodie, Eoin L., Williams, Kenneth H., & Beller, Harry R. Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer. United States. https://doi.org/10.1038/ismej.2016.25
Jewell, Talia N. M., Karaoz, Ulas, Brodie, Eoin L., Williams, Kenneth H., and Beller, Harry R. Fri .
"Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer". United States. https://doi.org/10.1038/ismej.2016.25. https://www.osti.gov/servlets/purl/1377452.
@article{osti_1377452,
title = {Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer},
author = {Jewell, Talia N. M. and Karaoz, Ulas and Brodie, Eoin L. and Williams, Kenneth H. and Beller, Harry R.},
abstractNote = {Groundwater ecosystems are conventionally thought to be fueled by surface-derived allochthonous organic matter and dominated by heterotrophic microbes living under often-oligotrophic conditions. However, in a 2-month study of nitrate amendment to a perennially suboxic aquifer in Rifle (CO), strain-resolved metatranscriptomic analysis revealed pervasive and diverse chemolithoautotrophic bacterial activity relevant to C, S, N and Fe cycling. Before nitrate injection, anaerobic ammonia-oxidizing (anammox) bacteria accounted for 16% of overall microbial community gene expression, whereas during the nitrate injection, two other groups of chemolithoautotrophic bacteria collectively accounted for 80% of the metatranscriptome: (1) members of the Fe(II)-oxidizing Gallionellaceae family and (2) strains of the S-oxidizing species, Sulfurimonas denitrificans. Notably, the proportion of the metatranscriptome accounted for by these three groups was considerably greater than the proportion of the metagenome coverage that they represented. Transcriptional analysis revealed some unexpected metabolic couplings, in particular, putative nitrate-dependent Fe(II) and S oxidation among nominally microaerophilic Gallionellaceae strains, including expression of periplasmic (NapAB) and membrane-bound (NarGHI) nitrate reductases. The three most active groups of chemolithoautotrophic bacteria in this study had overlapping metabolisms that allowed them to occupy different yet related metabolic niches throughout the study. Overall, these results highlight the important role that chemolithoautotrophy can have in aquifer biogeochemical cycling, a finding that has broad implications for understanding terrestrial carbon cycling and is supported by recent studies of geochemically diverse aquifers.},
doi = {10.1038/ismej.2016.25},
journal = {The ISME Journal},
number = 9,
volume = 10,
place = {United States},
year = {Fri Mar 04 00:00:00 EST 2016},
month = {Fri Mar 04 00:00:00 EST 2016}
}
Web of Science
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Insights into Carbon Metabolism Provided by Fluorescence In Situ Hybridization-Secondary Ion Mass Spectrometry Imaging of an Autotrophic, Nitrate-Reducing, Fe(II)-Oxidizing Enrichment Culture
journal, March 2018
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- Applied and Environmental Microbiology, Vol. 84, Issue 9
Growth and Population Dynamics of the Anaerobic Fe(II)-Oxidizing and Nitrate-Reducing Enrichment Culture KS
journal, March 2018
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- Applied and Environmental Microbiology, Vol. 84, Issue 9
Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome
journal, October 2018
- Wilmoth, Jared Lee; Moran, Mary Ann; Thompson, Aaron
- Microbiome, Vol. 6, Issue 1
Short-term effect of simulated salt marsh restoration by sand-amendment on sediment bacterial communities
journal, April 2019
- Thomas, François; Morris, James T.; Wigand, Cathleen
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Snowmelt Induced Hydrologic Perturbations Drive Dynamic Microbiological and Geochemical Behaviors across a Shallow Riparian Aquifer
journal, May 2016
- Danczak, Robert E.; Yabusaki, Steven B.; Williams, Kenneth H.
- Frontiers in Earth Science, Vol. 4
Evidence for Microbial Mediated NO3− Cycling Within Floodplain Sediments During Groundwater Fluctuations
journal, July 2019
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Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer
journal, January 2017
- Jewell, Talia N. M.; Karaoz, Ulas; Bill, Markus
- Frontiers in Microbiology, Vol. 8, Article No. 40
FeGenie: A Comprehensive Tool for the Identification of Iron Genes and Iron Gene Neighborhoods in Genome and Metagenome Assemblies
journal, January 2020
- Garber, Arkadiy I.; Nealson, Kenneth H.; Okamoto, Akihiro
- Frontiers in Microbiology, Vol. 11
Hidden diversity revealed by genome-resolved metagenomics of iron-oxidizing microbial mats from Lō’ihi Seamount, Hawai’i
journal, April 2017
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Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016
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Paired RNA Radiocarbon and Sequencing Analyses Indicate the Importance of Autotrophy in a Shallow Alluvial Aquifer
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Evidence for the Existence of Autotrophic Nitrate-Reducing Fe(II)-Oxidizing Bacteria in Marine Coastal Sediment
journal, October 2016
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- Applied and Environmental Microbiology, Vol. 82, Issue 20
Validating the Cyc2 Neutrophilic Iron Oxidation Pathway Using Meta-omics of Zetaproteobacteria Iron Mats at Marine Hydrothermal Vents
journal, February 2020
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Snowmelt Induced Hydrologic Perturbations Drive Dynamic Microbiological and Geochemical Behaviors across a Shallow Riparian Aquifer
journal, May 2016
- Danczak, Robert E.; Yabusaki, Steven B.; Williams, Kenneth H.
- Frontiers in Earth Science, Vol. 4
Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer
journal, January 2017
- Jewell, Talia N. M.; Karaoz, Ulas; Bill, Markus
- Frontiers in Microbiology, Vol. 8, Article No. 40
Probabilistic Modeling of Microbial Metabolic Networks for Integrating Partial Quantitative Knowledge Within the Nitrogen Cycle
journal, January 2019
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