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

doi:10.1073/pnas.1524915113

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

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 »

Authors:

Hood, Rachel D. ^[1] ; Higgins, Sean A. ^[1] ; Flamholz, Avi ^[1] ; Nichols, Robert J. ^[1] ;

Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
Univ. of California, Berkeley, CA (United States). Energy Biosciences Inst., Dept. of Molecular and Cell Biology and Dept. of Chemistry

Publication Date:: 2016-08-02

Grant/Contract Number:: SC0006394

Type:: 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)

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)

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

OSTI Identifier:: 1281325

Alternate Identifier(s):: OSTI ID: 1469295


                    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.,  
        Web.  doi:10.1073/pnas.1524915113.

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                    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.

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                    Hood, Rachel D., Higgins, Sean A., Flamholz, Avi, Nichols, Robert J., and Savage, David F.. 2016.  
        "The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus".  United States.  
        doi:10.1073/pnas.1524915113.

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@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         = {2016},

  month        = {8}

}

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Works referenced in this record:

Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus
journal, July 2009

Ito, H.; Mutsuda, M.; Murayama, Y.
Proceedings of the National Academy of Sciences, Vol. 106, Issue 33, p. 14168-14173
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Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different
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Lindahl, M.; Florencio, F. J.
Proceedings of the National Academy of Sciences, Vol. 100, Issue 26, p. 16107-16112
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The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli
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Traxler, Matthew F.; Summers, Sean M.; Nguyen, Huyen-Tran
Molecular Microbiology, Vol. 68, Issue 5, p. 1128-1148
DOI: 10.1111/j.1365-2958.2008.06229.x

HipA-Triggered Growth Arrest and β-Lactam Tolerance in Escherichia coli Are Mediated by RelA-Dependent ppGpp Synthesis
journal, May 2013

Bokinsky, G.; Baidoo, E. E. K.; Akella, S.
Journal of Bacteriology, Vol. 195, Issue 14, p. 3173-3182
DOI: 10.1128/JB.02210-12

Nutritional Control of Elongation of DNA Replication by (p)ppGpp
journal, March 2007

Wang, Jue D.; Sanders, Glenn M.; Grossman, Alan D.
Cell, Vol. 128, Issue 5, p. 865-875
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A One Pot, One Step, Precision Cloning Method with High Throughput Capability
journal, November 2008

Engler, Carola; Kandzia, Romy; Marillonnet, Sylvestre
PLoS ONE, Vol. 3, Issue 11, Article No. e3647
DOI: 10.1371/journal.pone.0003647

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