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Title: Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer

Abstract

Organic matter deposits in alluvial aquifers have been shown to result in the formation of naturally reduced zones (NRZs), which can modulate aquifer redox status and influence the speciation and mobility of metals, affecting groundwater geochemistry. In this study, we sought to better understand how natural organic matter fuels microbial communities within anoxic biogeochemical hot spots (NRZs) in a shallow alluvial aquifer at the Rifle (CO) site. We conducted a 20-day microcosm experiment in which NRZ sediments, which were enriched in buried woody plant material, served as the sole source of electron donors and microorganisms. The microcosms were constructed and incubated under anaerobic conditions in serum bottles with an initial N 2 headspace and were sampled every 5 days for metagenome and metatranscriptome profiles in combination with biogeochemical measurements. Biogeochemical data indicated that the decomposition of native organic matter occurred in different phases, beginning with mineralization of dissolved organic matter (DOM) to CO 2 during the first week of incubation, followed by a pulse of acetogenesis that dominated carbon flux after 2 weeks. A pulse of methanogenesis co-occurred with acetogenesis, but only accounted for a small fraction of carbon flux. The depletion of DOM over time was strongly correlated withmore » increases in expression of many genes associated with heterotrophy (e.g., amino acid, fatty acid, and carbohydrate metabolism) belonging to a Hydrogenophaga strain that accounted for a relatively large percentage (~8%) of the metatranscriptome. This Hydrogenophaga strain also expressed genes indicative of chemolithoautotrophy, including CO 2 fixation, H 2 oxidation, S-compound oxidation, and denitrification. The pulse of acetogenesis appears to have been collectively catalyzed by a number of different organisms and metabolisms, most prominently pyruvate:ferredoxin oxidoreductase. Unexpected genes were identified among the most highly expressed (>98th percentile) transcripts, including acetone carboxylase and cell-wall-associated hydrolases with unknown substrates (numerous lesser expressed cell-wall-associated hydrolases targeted peptidoglycan). Many of the most highly expressed hydrolases belonged to a Ca. Bathyarchaeota strain and may have been associated with recycling of bacterial biomass. Overall, these results highlight the complex nature of organic matter transformation in NRZs and the microbial metabolic pathways that interact to mediate redox status and elemental cycling.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1379690
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal Issue: JAN; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; strain-resolved metatranscriptome; metagenome; aquifer; naturally reduced zone (NRZ); Hydrogenophaga; Bathyarchaeota; biogeochemistry

Citation Formats

Jewell, Talia N. M., Karaoz, Ulas, Bill, Markus, Chakraborty, Romy, Brodie, Eoin L., Williams, Kenneth H., and Beller, Harry R. Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.00040.
Jewell, Talia N. M., Karaoz, Ulas, Bill, Markus, Chakraborty, Romy, Brodie, Eoin L., Williams, Kenneth H., & Beller, Harry R. Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer. United States. doi:10.3389/fmicb.2017.00040.
Jewell, Talia N. M., Karaoz, Ulas, Bill, Markus, Chakraborty, Romy, Brodie, Eoin L., Williams, Kenneth H., and Beller, Harry R. Wed . "Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer". United States. doi:10.3389/fmicb.2017.00040. https://www.osti.gov/servlets/purl/1379690.
@article{osti_1379690,
title = {Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer},
author = {Jewell, Talia N. M. and Karaoz, Ulas and Bill, Markus and Chakraborty, Romy and Brodie, Eoin L. and Williams, Kenneth H. and Beller, Harry R.},
abstractNote = {Organic matter deposits in alluvial aquifers have been shown to result in the formation of naturally reduced zones (NRZs), which can modulate aquifer redox status and influence the speciation and mobility of metals, affecting groundwater geochemistry. In this study, we sought to better understand how natural organic matter fuels microbial communities within anoxic biogeochemical hot spots (NRZs) in a shallow alluvial aquifer at the Rifle (CO) site. We conducted a 20-day microcosm experiment in which NRZ sediments, which were enriched in buried woody plant material, served as the sole source of electron donors and microorganisms. The microcosms were constructed and incubated under anaerobic conditions in serum bottles with an initial N2 headspace and were sampled every 5 days for metagenome and metatranscriptome profiles in combination with biogeochemical measurements. Biogeochemical data indicated that the decomposition of native organic matter occurred in different phases, beginning with mineralization of dissolved organic matter (DOM) to CO2 during the first week of incubation, followed by a pulse of acetogenesis that dominated carbon flux after 2 weeks. A pulse of methanogenesis co-occurred with acetogenesis, but only accounted for a small fraction of carbon flux. The depletion of DOM over time was strongly correlated with increases in expression of many genes associated with heterotrophy (e.g., amino acid, fatty acid, and carbohydrate metabolism) belonging to a Hydrogenophaga strain that accounted for a relatively large percentage (~8%) of the metatranscriptome. This Hydrogenophaga strain also expressed genes indicative of chemolithoautotrophy, including CO2 fixation, H2 oxidation, S-compound oxidation, and denitrification. The pulse of acetogenesis appears to have been collectively catalyzed by a number of different organisms and metabolisms, most prominently pyruvate:ferredoxin oxidoreductase. Unexpected genes were identified among the most highly expressed (>98th percentile) transcripts, including acetone carboxylase and cell-wall-associated hydrolases with unknown substrates (numerous lesser expressed cell-wall-associated hydrolases targeted peptidoglycan). Many of the most highly expressed hydrolases belonged to a Ca. Bathyarchaeota strain and may have been associated with recycling of bacterial biomass. Overall, these results highlight the complex nature of organic matter transformation in NRZs and the microbial metabolic pathways that interact to mediate redox status and elemental cycling.},
doi = {10.3389/fmicb.2017.00040},
journal = {Frontiers in Microbiology},
number = JAN,
volume = 8,
place = {United States},
year = {Wed Jan 25 00:00:00 EST 2017},
month = {Wed Jan 25 00:00:00 EST 2017}
}

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