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Title: Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm

Abstract

Increasing anthropogenic inputs of fixed nitrogen are leading to greater eutrophication of aquatic environments, but it is unclear how this impacts the flux and fate of carbon in lacustrine and riverine systems. Here, we present evidence that the form of nitrogen governs the partitioning of carbon among members in a genome-sequenced, model phototrophic biofilm of 20 members. Consumption of NO3 as the sole nitrogen source unexpectedly resulted in more rapid transfer of carbon to heterotrophs than when NH4+ was also provided, suggesting alterations in the form of carbon exchanged. The form of nitrogen dramatically impacted net community nitrogen, but not carbon, uptake rates. Furthermore, this alteration in nitrogen form caused very large but focused alterations to community structure, strongly impacting the abundance of only two species within the biofilm and modestly impacting a third member species. Our data suggest that nitrogen metabolism may coordinate coupled carbon-nitrogen biogeochemical cycling in benthic biofilms and, potentially, in phototroph-heterotroph consortia more broadly. It further indicates that the form of nitrogen inputs may significantly impact the contribution of these communities to carbon partitioning across the terrestrial-aquatic interface.

Authors:
ORCiD logo; ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1632235
Alternate Identifier(s):
OSTI ID: 1647036
Report Number(s):
PNNL-SA-145330
Journal ID: ISSN 2379-5077; e00260-20; /msystems/5/3/msys.00260-20.atom
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Name: mSystems Journal Volume: 5 Journal Issue: 3; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
carbon cycling; cyanobacteria; mass spectrometry; nitrogen cycling; stable isotopes

Citation Formats

Anderton, Christopher R., Mobberley, Jennifer M., Cole, Jessica K., Nunez, Jamie R., Starke, Robert, Boaro, Amy A., Yesiltepe, Yasemin, Morton, Beau R., Cory, Alexandra B., Cardamone, Hayley C., Hofmockel, Kirsten S., Lipton, Mary S., Moran, James J., Renslow, Ryan S., Fredrickson, James K., Lindemann, Stephen R., and Hallam, ed., Steven J. Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm. United States: N. p., 2020. Web. doi:10.1128/mSystems.00260-20.
Anderton, Christopher R., Mobberley, Jennifer M., Cole, Jessica K., Nunez, Jamie R., Starke, Robert, Boaro, Amy A., Yesiltepe, Yasemin, Morton, Beau R., Cory, Alexandra B., Cardamone, Hayley C., Hofmockel, Kirsten S., Lipton, Mary S., Moran, James J., Renslow, Ryan S., Fredrickson, James K., Lindemann, Stephen R., & Hallam, ed., Steven J. Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm. United States. doi:https://doi.org/10.1128/mSystems.00260-20
Anderton, Christopher R., Mobberley, Jennifer M., Cole, Jessica K., Nunez, Jamie R., Starke, Robert, Boaro, Amy A., Yesiltepe, Yasemin, Morton, Beau R., Cory, Alexandra B., Cardamone, Hayley C., Hofmockel, Kirsten S., Lipton, Mary S., Moran, James J., Renslow, Ryan S., Fredrickson, James K., Lindemann, Stephen R., and Hallam, ed., Steven J. Tue . "Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm". United States. doi:https://doi.org/10.1128/mSystems.00260-20.
@article{osti_1632235,
title = {Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm},
author = {Anderton, Christopher R. and Mobberley, Jennifer M. and Cole, Jessica K. and Nunez, Jamie R. and Starke, Robert and Boaro, Amy A. and Yesiltepe, Yasemin and Morton, Beau R. and Cory, Alexandra B. and Cardamone, Hayley C. and Hofmockel, Kirsten S. and Lipton, Mary S. and Moran, James J. and Renslow, Ryan S. and Fredrickson, James K. and Lindemann, Stephen R. and Hallam, ed., Steven J.},
abstractNote = {Increasing anthropogenic inputs of fixed nitrogen are leading to greater eutrophication of aquatic environments, but it is unclear how this impacts the flux and fate of carbon in lacustrine and riverine systems. Here, we present evidence that the form of nitrogen governs the partitioning of carbon among members in a genome-sequenced, model phototrophic biofilm of 20 members. Consumption of NO3– as the sole nitrogen source unexpectedly resulted in more rapid transfer of carbon to heterotrophs than when NH4+ was also provided, suggesting alterations in the form of carbon exchanged. The form of nitrogen dramatically impacted net community nitrogen, but not carbon, uptake rates. Furthermore, this alteration in nitrogen form caused very large but focused alterations to community structure, strongly impacting the abundance of only two species within the biofilm and modestly impacting a third member species. Our data suggest that nitrogen metabolism may coordinate coupled carbon-nitrogen biogeochemical cycling in benthic biofilms and, potentially, in phototroph-heterotroph consortia more broadly. It further indicates that the form of nitrogen inputs may significantly impact the contribution of these communities to carbon partitioning across the terrestrial-aquatic interface.},
doi = {10.1128/mSystems.00260-20},
journal = {mSystems},
number = 3,
volume = 5,
place = {United States},
year = {2020},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
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DOI: https://doi.org/10.1128/mSystems.00260-20

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