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Title: Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community

Abstract

Stimulation of subsurface microorganisms to induce reductive immobilization of metals is a promising approach for bioremediation, yet the overall microbial community response is typically poorly understood. Here we used community proteogenomics to test the hypothesis that excess input of acetate activates syntrophic interactions among autotrophs and heterotrophs. A flow-through sediment column was incubated in a groundwater well of an acetate-amended aquifer. Genomic sequences from the community recovered during microbial sulfate reduction were used to econstruct, de novo, near-complete genomes for Desulfobacter (Deltaproteobacteria) and relatives of Sulfurovum and Sulfurimonas (Epsilonproteobacteria), and Bacteroidetes. Partial genomes were obtained for Clostridiales (Firmicutes) and Desulfuromonadales-like Deltaproteobacteria. The majority of proteins identified by mass spectrometry corresponded to Desulfobacter-like species, and demonstrate the role of this organism in sulfate reduction (Dsr and APS), nitrogen-fixation (Nif) and acetate oxidation to CO2 during amendment. Results suggest less abundant Desulfuromonadales and Bacteroidetes also actively contributed to CO2 production via the TCA cycle. Proteomic data indicate that sulfide was partially re-oxidized by Epsilonproteobacteria through nitrate-dependent sulfide oxidation (using Nap, Nir, Nos, SQR and Sox), with CO2 fixed using the reverse TCA cycle. Modeling shows that this reaction was thermodynamically possible, and kinetically favorable relative to acetate-dependent denitrification. We conclude that high-levelsmore » of carbon amendment aimed to stimulate anaerobic heterotrophy led to carbon fixation in co-dependent chemoautotrophs. These results have implications for understanding complex ecosystem behavior, and show that high levels of organic carbon supplementation can expand the range of microbial functionalities accessible for ecosystem manipulation.« less

Authors:
 [1];  [2];  [3];  [1];  [3];  [1];  [1];  [2];  [1];  [2];  [4];  [1]
  1. University of California, Berkeley
  2. ORNL
  3. Lawrence Berkeley National Laboratory (LBNL)
  4. Pacific Northwest National Laboratory (PNNL)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
Work for Others (WFO)
OSTI Identifier:
1088112
DOE Contract Number:  
DE-AC05-00OR22725
Resource Type:
Journal Article
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 7; Journal Issue: 4; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
metagenomics/proteomics/subsurface/sediment/syntrophy/autotroph

Citation Formats

Handley, KM, Verberkmoes, Nathan C, Steefel, Carl I, Sharon, I, Williams, Ken, Miller, CS, Frischkorn, Kyle C, Chourey, Karuna, Thomas, Brian, Shah, Manesh B, Long, Phil, Hettich, Robert, and Banfield, Jillian F. Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community. United States: N. p., 2013. Web. doi:10.1038/ismej.2012.148.
Handley, KM, Verberkmoes, Nathan C, Steefel, Carl I, Sharon, I, Williams, Ken, Miller, CS, Frischkorn, Kyle C, Chourey, Karuna, Thomas, Brian, Shah, Manesh B, Long, Phil, Hettich, Robert, & Banfield, Jillian F. Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community. United States. https://doi.org/10.1038/ismej.2012.148
Handley, KM, Verberkmoes, Nathan C, Steefel, Carl I, Sharon, I, Williams, Ken, Miller, CS, Frischkorn, Kyle C, Chourey, Karuna, Thomas, Brian, Shah, Manesh B, Long, Phil, Hettich, Robert, and Banfield, Jillian F. 2013. "Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community". United States. https://doi.org/10.1038/ismej.2012.148.
@article{osti_1088112,
title = {Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community},
author = {Handley, KM and Verberkmoes, Nathan C and Steefel, Carl I and Sharon, I and Williams, Ken and Miller, CS and Frischkorn, Kyle C and Chourey, Karuna and Thomas, Brian and Shah, Manesh B and Long, Phil and Hettich, Robert and Banfield, Jillian F.},
abstractNote = {Stimulation of subsurface microorganisms to induce reductive immobilization of metals is a promising approach for bioremediation, yet the overall microbial community response is typically poorly understood. Here we used community proteogenomics to test the hypothesis that excess input of acetate activates syntrophic interactions among autotrophs and heterotrophs. A flow-through sediment column was incubated in a groundwater well of an acetate-amended aquifer. Genomic sequences from the community recovered during microbial sulfate reduction were used to econstruct, de novo, near-complete genomes for Desulfobacter (Deltaproteobacteria) and relatives of Sulfurovum and Sulfurimonas (Epsilonproteobacteria), and Bacteroidetes. Partial genomes were obtained for Clostridiales (Firmicutes) and Desulfuromonadales-like Deltaproteobacteria. The majority of proteins identified by mass spectrometry corresponded to Desulfobacter-like species, and demonstrate the role of this organism in sulfate reduction (Dsr and APS), nitrogen-fixation (Nif) and acetate oxidation to CO2 during amendment. Results suggest less abundant Desulfuromonadales and Bacteroidetes also actively contributed to CO2 production via the TCA cycle. Proteomic data indicate that sulfide was partially re-oxidized by Epsilonproteobacteria through nitrate-dependent sulfide oxidation (using Nap, Nir, Nos, SQR and Sox), with CO2 fixed using the reverse TCA cycle. Modeling shows that this reaction was thermodynamically possible, and kinetically favorable relative to acetate-dependent denitrification. We conclude that high-levels of carbon amendment aimed to stimulate anaerobic heterotrophy led to carbon fixation in co-dependent chemoautotrophs. These results have implications for understanding complex ecosystem behavior, and show that high levels of organic carbon supplementation can expand the range of microbial functionalities accessible for ecosystem manipulation.},
doi = {10.1038/ismej.2012.148},
url = {https://www.osti.gov/biblio/1088112}, journal = {The ISME Journal},
issn = {1751-7362},
number = 4,
volume = 7,
place = {United States},
year = {Tue Jan 01 00:00:00 EST 2013},
month = {Tue Jan 01 00:00:00 EST 2013}
}