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Title: The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus

Abstract

The cyanobacterium Synechococcus elongatus relies upon photosynthesis to drive metabolism and growth. During darkness, Synechococcus stops growing, derives energy from its glycogen stores, and greatly decreases rates of macromolecular synthesis via unknown mechanisms. In this work, we show that the stringent response, a stress response pathway whose genes are conserved across bacteria and plant plastids, contributes to this dark adaptation. Levels of the stringent response alarmone guanosine 3'-diphosphate 5'-diphosphate (ppGpp) rise after a shift from light to dark, indicating that darkness triggers the same response in cyanobacteria as starvation in heterotrophic bacteria. High levels of ppGpp are sufficient to stop growth and dramatically alter many aspects of cellular physiology, including levels of photosynthetic pigments and polyphosphate, DNA content, and the rate of translation. Cells unable to synthesize ppGpp display pronounced growth defects after exposure to darkness. The stringent response regulates expression of a number of genes in Synechococcus, including ribosomal hibernation promoting factor ( hpf), which causes ribosomes to dimerize in the dark and may contribute to decreased translation. Although the metabolism of Synechococcus differentiates it from other model bacterial systems, the logic of the stringent response remains remarkably conserved, while at the same time having adapted to the uniquemore » stresses of the photosynthetic lifestyle.« less

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [2]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
  2. Univ. of California, Berkeley, CA (United States). Energy Biosciences Inst., Dept. of Molecular and Cell Biology and Dept. of Chemistry
Publication Date:
Research Org.:
Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); Sloan Foundation; National Science Foundation (NSF)
OSTI Identifier:
1281325
Alternate Identifier(s):
OSTI ID: 1469295
Grant/Contract Number:  
SC0006394
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 33; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; cyanobacteria; Synechococcus; stringent response; (p)ppGpp; hibernation promoting factor

Citation Formats

Hood, Rachel D., Higgins, Sean A., Flamholz, Avi, Nichols, Robert J., and Savage, David F. The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus. United States: N. p., 2016. Web. doi:10.1073/pnas.1524915113.
Hood, Rachel D., Higgins, Sean A., Flamholz, Avi, Nichols, Robert J., & Savage, David F. The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus. United States. doi:10.1073/pnas.1524915113.
Hood, Rachel D., Higgins, Sean A., Flamholz, Avi, Nichols, Robert J., and Savage, David F. Tue . "The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus". United States. doi:10.1073/pnas.1524915113.
@article{osti_1281325,
title = {The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus},
author = {Hood, Rachel D. and Higgins, Sean A. and Flamholz, Avi and Nichols, Robert J. and Savage, David F.},
abstractNote = {The cyanobacterium Synechococcus elongatus relies upon photosynthesis to drive metabolism and growth. During darkness, Synechococcus stops growing, derives energy from its glycogen stores, and greatly decreases rates of macromolecular synthesis via unknown mechanisms. In this work, we show that the stringent response, a stress response pathway whose genes are conserved across bacteria and plant plastids, contributes to this dark adaptation. Levels of the stringent response alarmone guanosine 3'-diphosphate 5'-diphosphate (ppGpp) rise after a shift from light to dark, indicating that darkness triggers the same response in cyanobacteria as starvation in heterotrophic bacteria. High levels of ppGpp are sufficient to stop growth and dramatically alter many aspects of cellular physiology, including levels of photosynthetic pigments and polyphosphate, DNA content, and the rate of translation. Cells unable to synthesize ppGpp display pronounced growth defects after exposure to darkness. The stringent response regulates expression of a number of genes in Synechococcus, including ribosomal hibernation promoting factor (hpf), which causes ribosomes to dimerize in the dark and may contribute to decreased translation. Although the metabolism of Synechococcus differentiates it from other model bacterial systems, the logic of the stringent response remains remarkably conserved, while at the same time having adapted to the unique stresses of the photosynthetic lifestyle.},
doi = {10.1073/pnas.1524915113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 33,
volume = 113,
place = {United States},
year = {Tue Aug 02 00:00:00 EDT 2016},
month = {Tue Aug 02 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1524915113

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

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