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Title: Stoichiometric Network Analysis of Cyanobacterial Acclimation to Photosynthesis-Associated Stresses Identifies Heterotrophic Niches

Abstract

Metabolic acclimation to photosynthesis-associated stresses was examined in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 using integrated computational and photobioreactor analyses. A genome-enabled metabolic model, complete with measured biomass composition, was analyzed using ecological resource allocation theory to predict and interpret metabolic acclimation to irradiance, O 2, and nutrient stresses. Reduced growth efficiency, shifts in photosystem utilization, changes in photorespiration strategies, and differing byproduct secretion patterns were predicted to occur along culturing stress gradients. These predictions were compared with photobioreactor physiological data and previously published transcriptomic data and found to be highly consistent with observations, providing a systems-based rationale for the culture phenotypes. The analysis also indicated that cyanobacterial stress acclimation strategies created niches for heterotrophic organisms and that heterotrophic activity could enhance cyanobacterial stress tolerance by removing inhibitory metabolic byproducts. This study provides mechanistic insight into stress acclimation strategies in photoautotrophs and establishes a framework for predicting, designing, and engineering both axenic and photoautotrophic-heterotrophic systems as a function of controllable parameters.

Authors:
 [1]; ORCiD logo [2];  [3]
  1. Montana State Univ., Bozeman, MT (United States). Microbiology and Immunology, Center for Biofilm Engineering
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
  3. Montana State Univ., Bozeman, MT (United States). Chemical and Biological Engineering, Center for Biofilm Engineering
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) (SC-23)
OSTI Identifier:
1367375
Report Number(s):
PNNL-SA-123196
Journal ID: ISSN 2227-9717; 49356; KP1601010
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Processes
Additional Journal Information:
Journal Volume: 5; Journal Issue: 2; Journal ID: ISSN 2227-9717
Publisher:
Multidisciplinary Digital Publishing Institute (MDPI)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; cross-feeding; cyanobacteria; elementary flux mode analysis; irradiance; resource allocation; RuBisCO; stress acclimation; Environmental Molecular Sciences Laboratory

Citation Formats

Beck, Ashley, Bernstein, Hans, and Carlson, Ross. Stoichiometric Network Analysis of Cyanobacterial Acclimation to Photosynthesis-Associated Stresses Identifies Heterotrophic Niches. United States: N. p., 2017. Web. doi:10.3390/pr5020032.
Beck, Ashley, Bernstein, Hans, & Carlson, Ross. Stoichiometric Network Analysis of Cyanobacterial Acclimation to Photosynthesis-Associated Stresses Identifies Heterotrophic Niches. United States. doi:10.3390/pr5020032.
Beck, Ashley, Bernstein, Hans, and Carlson, Ross. Mon . "Stoichiometric Network Analysis of Cyanobacterial Acclimation to Photosynthesis-Associated Stresses Identifies Heterotrophic Niches". United States. doi:10.3390/pr5020032. https://www.osti.gov/servlets/purl/1367375.
@article{osti_1367375,
title = {Stoichiometric Network Analysis of Cyanobacterial Acclimation to Photosynthesis-Associated Stresses Identifies Heterotrophic Niches},
author = {Beck, Ashley and Bernstein, Hans and Carlson, Ross},
abstractNote = {Metabolic acclimation to photosynthesis-associated stresses was examined in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 using integrated computational and photobioreactor analyses. A genome-enabled metabolic model, complete with measured biomass composition, was analyzed using ecological resource allocation theory to predict and interpret metabolic acclimation to irradiance, O2, and nutrient stresses. Reduced growth efficiency, shifts in photosystem utilization, changes in photorespiration strategies, and differing byproduct secretion patterns were predicted to occur along culturing stress gradients. These predictions were compared with photobioreactor physiological data and previously published transcriptomic data and found to be highly consistent with observations, providing a systems-based rationale for the culture phenotypes. The analysis also indicated that cyanobacterial stress acclimation strategies created niches for heterotrophic organisms and that heterotrophic activity could enhance cyanobacterial stress tolerance by removing inhibitory metabolic byproducts. This study provides mechanistic insight into stress acclimation strategies in photoautotrophs and establishes a framework for predicting, designing, and engineering both axenic and photoautotrophic-heterotrophic systems as a function of controllable parameters.},
doi = {10.3390/pr5020032},
journal = {Processes},
number = 2,
volume = 5,
place = {United States},
year = {Mon Jun 19 00:00:00 EDT 2017},
month = {Mon Jun 19 00:00:00 EDT 2017}
}

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Works referenced in this record:

Complete Genome Structure of the Thermophilic Cyanobacterium Thermosynechococcus elongatus BP-1
journal, January 2002