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

Abstract

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, Colorado, USA, and document interlinked microbial roles in geochemical cycling. The organic carbon content in the aquifer was elevated via two acetate-based biostimulation treatments. 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 genomes from a new phylum (ACD20), phylogenetically novel members of the Chloroflexi and Bacteroidetes, 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 currency in the subsurface. Our proteogenomic data further indicate the consumption of fermentation intermediates by Proteobacteria can bemore » coupled to nitrate, sulfate, and iron reduction. Thus, fermentation carried out by previously unstudied members of sediment microbial communities may be an important driver of diverse subsurface biogeochemical cycles.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1171894
Report Number(s):
PNNL-SA-97151
830403000
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
The ISME Journal, 8(7):1452-1463
Additional Journal Information:
Journal Name: The ISME Journal, 8(7):1452-1463
Country of Publication:
United States
Language:
English
Subject:
metabolic interdependencies; phylogenetically novel fermenters; respiratory organisms; unconfined aquifer

Citation Formats

Wrighton, Kelly C., Castelle, Cindy, Wilkins, Michael J., Hug, Laura A., Sharon, I., Thomas, Brian C., Handley, Kim M., Mullin, Sean W., Nicora, Carrie D., Singh, Andrea, Lipton, Mary S., Long, Philip E., Williams, Kenneth H., and Banfield, Jillian F. Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. United States: N. p., 2014. Web. doi:10.1038/ismej.2013.249.
Wrighton, Kelly C., Castelle, Cindy, Wilkins, Michael J., Hug, Laura A., Sharon, I., Thomas, Brian C., Handley, Kim M., Mullin, Sean W., Nicora, Carrie D., Singh, Andrea, Lipton, Mary S., Long, Philip E., Williams, Kenneth H., & Banfield, Jillian F. Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. United States. https://doi.org/10.1038/ismej.2013.249
Wrighton, Kelly C., Castelle, Cindy, Wilkins, Michael J., Hug, Laura A., Sharon, I., Thomas, Brian C., Handley, Kim M., Mullin, Sean W., Nicora, Carrie D., Singh, Andrea, Lipton, Mary S., Long, Philip E., Williams, Kenneth H., and Banfield, Jillian F. 2014. "Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer". United States. https://doi.org/10.1038/ismej.2013.249.
@article{osti_1171894,
title = {Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer},
author = {Wrighton, Kelly C. and Castelle, Cindy and Wilkins, Michael J. and Hug, Laura A. and Sharon, I. and Thomas, Brian C. and Handley, Kim M. and Mullin, Sean W. and Nicora, Carrie D. and Singh, Andrea and Lipton, Mary S. and Long, Philip E. and Williams, Kenneth H. and Banfield, Jillian F.},
abstractNote = {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, Colorado, USA, and document interlinked microbial roles in geochemical cycling. The organic carbon content in the aquifer was elevated via two acetate-based biostimulation treatments. 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 genomes from a new phylum (ACD20), phylogenetically novel members of the Chloroflexi and Bacteroidetes, 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 currency 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 unstudied members of sediment microbial communities may be an important driver of diverse subsurface biogeochemical cycles.},
doi = {10.1038/ismej.2013.249},
url = {https://www.osti.gov/biblio/1171894}, journal = {The ISME Journal, 8(7):1452-1463},
number = ,
volume = ,
place = {United States},
year = {Tue Jul 08 00:00:00 EDT 2014},
month = {Tue Jul 08 00:00:00 EDT 2014}
}