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Title: Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm

Abstract

Although it is becoming clear that many microbial primary producers can also play a role as organic consumers, we know very little about the metabolic regulation of photoautotroph organic matter consumption. Cyanobacteria in phototrophic biofilms can reuse extracellular organic carbon, but the metabolic drivers of extracellular processes are surprisingly complex. We investigated the metabolic foundations of organic matter reuse by comparing exoproteome composition and incorporation of 13C-labeled and 15N-labeled cyanobacterial extracellular organic matter (EOM) in a unicyanobacterial biofilm incubated using different light regimes. In the light and the dark, cyanobacterial direct organic C assimilation accounted for 32% and 43%, respectively, of all organic C assimilation in the community. Under photosynthesis conditions, we measured increased excretion of extracellular polymeric substances (EPS) and proteins involved in micronutrient transport, suggesting that requirements for micronutrients may drive EOM assimilation during daylight hours. This interpretation was supported by photosynthesis inhibition experiments, in which cyanobacteria incorporated N-rich EOM-derived material. In contrast, under dark, C-starved conditions, cyanobacteria incorporated C-rich EOM-derived organic matter, decreased excretion of EPS, and showed an increased abundance of degradative exoproteins, demonstrating the use of the extracellular domain for C storage. Sequence-structure modeling of one of these exoproteins predicted a specific hydrolytic activity thatmore » was subsequently detected, confirming increased EOM degradation in the dark. Associated heterotrophic bacteria increased in abundance and upregulated transport proteins under dark relative to light conditions. Taken together, our results indicate that biofilm cyanobacteria are successful competitors for organic C and N and that cyanobacterial nutrient and energy requirements control the use of EOM. IMPORTANCECyanobacteria are globally distributed primary producers, and the fate of their fixed C influences microbial biogeochemical cycling. This fate is complicated by cyanobacterial degradation and assimilation of organic matter, but because cyanobacteria are assumed to be poor competitors for organic matter consumption, regulation of this process is not well tested. In mats and biofilms, this is especially relevant because cyanobacteria produce an extensive organic extracellular matrix, providing the community with a rich source of nutrients. Light is a well-known regulator of cyanobacterial metabolism, so we characterized the effects of light availability on the incorporation of organic matter. Using stable isotope tracing at the single-cell level, we quantified photoautotroph assimilation under different metabolic conditions and integrated the results with proteomics to elucidate metabolic status. We found that cyanobacteria effectively compete for organic matter in the light and the dark and that nutrient requirements and community interactions contribute to cycling of extracellular organic matter.« less

Authors:
; ; ; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1342324
Report Number(s):
PNNL-SA-121065
Journal ID: ISSN 2150-7511; KP1601010
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Volume: 7; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Stuart, Rhona K., Mayali, Xavier, Boaro, Amy A., Zemla, Adam, Everroad, R. Craig, Nilson, Daniel, Weber, Peter K., Lipton, Mary, Bebout, Brad M., Pett-Ridge, Jennifer, and Thelen, Michael P. Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm. United States: N. p., 2016. Web. doi:10.1128/mBio.00650-16.
Stuart, Rhona K., Mayali, Xavier, Boaro, Amy A., Zemla, Adam, Everroad, R. Craig, Nilson, Daniel, Weber, Peter K., Lipton, Mary, Bebout, Brad M., Pett-Ridge, Jennifer, & Thelen, Michael P. Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm. United States. https://doi.org/10.1128/mBio.00650-16
Stuart, Rhona K., Mayali, Xavier, Boaro, Amy A., Zemla, Adam, Everroad, R. Craig, Nilson, Daniel, Weber, Peter K., Lipton, Mary, Bebout, Brad M., Pett-Ridge, Jennifer, and Thelen, Michael P. Tue . "Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm". United States. https://doi.org/10.1128/mBio.00650-16.
@article{osti_1342324,
title = {Light Regimes Shape Utilization of Extracellular Organic C and N in a Cyanobacterial Biofilm},
author = {Stuart, Rhona K. and Mayali, Xavier and Boaro, Amy A. and Zemla, Adam and Everroad, R. Craig and Nilson, Daniel and Weber, Peter K. and Lipton, Mary and Bebout, Brad M. and Pett-Ridge, Jennifer and Thelen, Michael P.},
abstractNote = {Although it is becoming clear that many microbial primary producers can also play a role as organic consumers, we know very little about the metabolic regulation of photoautotroph organic matter consumption. Cyanobacteria in phototrophic biofilms can reuse extracellular organic carbon, but the metabolic drivers of extracellular processes are surprisingly complex. We investigated the metabolic foundations of organic matter reuse by comparing exoproteome composition and incorporation of13C-labeled and15N-labeled cyanobacterial extracellular organic matter (EOM) in a unicyanobacterial biofilm incubated using different light regimes. In the light and the dark, cyanobacterial direct organic C assimilation accounted for 32% and 43%, respectively, of all organic C assimilation in the community. Under photosynthesis conditions, we measured increased excretion of extracellular polymeric substances (EPS) and proteins involved in micronutrient transport, suggesting that requirements for micronutrients may drive EOM assimilation during daylight hours. This interpretation was supported by photosynthesis inhibition experiments, in which cyanobacteria incorporated N-rich EOM-derived material. In contrast, under dark, C-starved conditions, cyanobacteria incorporated C-rich EOM-derived organic matter, decreased excretion of EPS, and showed an increased abundance of degradative exoproteins, demonstrating the use of the extracellular domain for C storage. Sequence-structure modeling of one of these exoproteins predicted a specific hydrolytic activity that was subsequently detected, confirming increased EOM degradation in the dark. Associated heterotrophic bacteria increased in abundance and upregulated transport proteins under dark relative to light conditions. Taken together, our results indicate that biofilm cyanobacteria are successful competitors for organic C and N and that cyanobacterial nutrient and energy requirements control the use of EOM. IMPORTANCECyanobacteria are globally distributed primary producers, and the fate of their fixed C influences microbial biogeochemical cycling. This fate is complicated by cyanobacterial degradation and assimilation of organic matter, but because cyanobacteria are assumed to be poor competitors for organic matter consumption, regulation of this process is not well tested. In mats and biofilms, this is especially relevant because cyanobacteria produce an extensive organic extracellular matrix, providing the community with a rich source of nutrients. Light is a well-known regulator of cyanobacterial metabolism, so we characterized the effects of light availability on the incorporation of organic matter. Using stable isotope tracing at the single-cell level, we quantified photoautotroph assimilation under different metabolic conditions and integrated the results with proteomics to elucidate metabolic status. We found that cyanobacteria effectively compete for organic matter in the light and the dark and that nutrient requirements and community interactions contribute to cycling of extracellular organic matter.},
doi = {10.1128/mBio.00650-16},
url = {https://www.osti.gov/biblio/1342324}, journal = {mBio (Online)},
issn = {2150-7511},
number = 3,
volume = 7,
place = {United States},
year = {2016},
month = {6}
}

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