Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels

Murton, Jaclyn; Nagarajan, Aparna; Nguyen, Amelia Y.; Liberton, Michelle; Hancock, Harmony A.; Pakrasi, Himadri B.; Timlin, Jerilyn A.

doi:10.1007/s11120-017-0422-7

Title: Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels

Journal Article · 21 July 2017 · Photosynthesis Research

DOI: https://doi.org/10.1007/s11120-017-0422-7 · OSTI ID:1372115

Murton, Jaclyn ^[1];

^[2];

^[3]; Liberton, Michelle ^[4];

^[5];

^[4];

^[1]

Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Washington Univ., St. Louis, MO (United States); Univ. of Colorado, Boulder, CO (United States)
Washington Univ., St. Louis, MO (United States); United States Environmental Protection Agency, Washington, D.C. (United States)
Washington Univ., St. Louis, MO (United States)
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States); Old Dominion Univ., Norfolk, VA (United States)

Cyanobacterial phycobilisome (PBS) pigment-protein complexes harvest light and transfer the energy to reaction centers. Previous ensemble studies have shown that cyanobacteria respond to changes in nutrient availability by modifying the structure of PBS complexes, but this process has not been visualized for individual pigments at the single-cell level due to spectral overlap. We characterized the response of four key photosynthetic pigments to nitrogen depletion and repletion at the subcellular level in individual, live Synechocystis sp. PCC 6803 cells using hyperspectral confocal fluorescence microscopy and multivariate image analysis. Our results revealed that PBS degradation and re-synthesis comprise a rapid response to nitrogen fluctuations, with coordinated populations of cells undergoing pigment modifications. Chlorophyll fluorescence originating from photosystem I and II decreased during nitrogen starvation, but no alteration in subcellular chlorophyll localization was found. Lastly, we observed differential rod and core pigment responses to nitrogen deprivation, suggesting that PBS complexes undergo a stepwise degradation process.

View Journal Article

Cite

Export

Save

Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE

Grant/Contract Number:: AC04-94AL85000; SC0001035; NA0003525

OSTI ID:: 1372115

Alternate ID(s):: OSTI ID: 1374747

Report Number(s):: SAND-2017-7775J; PII: 422

Journal Information:: Photosynthesis Research, Vol. 134, Issue 2; ISSN 0166-8595

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (42)

A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. Collier, J. L.; Grossman, A. R. The EMBO Journal, Vol. 13, Issue 5 https://doi.org/10.1002/j.1460-2075.1994.tb06352.x	journal	March 1994
Green Autofluorescence in Dinoflagellates, Diatoms, and Other Microalgae and Its Implications for Vital Staining and Morphological Studies Tang, Y. Z.; Dobbs, F. C. Applied and Environmental Microbiology, Vol. 73, Issue 7 https://doi.org/10.1128/aem.01741-06	journal	February 2007
Global Proteomics Reveal an Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations Wegener, Kimberly M.; Singh, Abhay K.; Jacobs, Jon M. Molecular & Cellular Proteomics, Vol. 9, Issue 12 https://doi.org/10.1074/mcp.M110.000109	journal	September 2010
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates Allen, Mary Mennes Journal of Phycology, Vol. 4, Issue 1 https://doi.org/10.1111/j.1529-8817.1968.tb04667.x	journal	March 1968
Expression of two nblA -homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803 Baier, Kerstin; Nicklisch, Sabine; Grundner, Christoph FEMS Microbiology Letters, Vol. 195, Issue 1 https://doi.org/10.1111/j.1574-6968.2001.tb10494.x	journal	February 2001
Preprocessing strategies to improve MCR analyses of hyperspectral images Jones, Howland D.T.; Haaland, David M.; Sinclair, Michael B. Chemometrics and Intelligent Laboratory Systems, Vol. 117, p. 149-158 https://doi.org/10.1016/j.chemolab.2012.01.011	journal	August 2012
Tracking the Light Environment by Cyanobacteria and the Dynamic Nature of Light Harvesting Grossman, Arthur R.; Bhaya, Devaki; He, Qingfang Journal of Biological Chemistry, Vol. 276, Issue 15 https://doi.org/10.1074/jbc.R100003200	journal	February 2001
Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. Collier, J. L.; Grossman, A. R. Journal of Bacteriology, Vol. 174, Issue 14 https://doi.org/10.1128/jb.174.14.4718-4726.1992	journal	July 1992
Awakening of a Dormant Cyanobacterium from Nitrogen Chlorosis Reveals a Genetically Determined Program Klotz, Alexander; Georg, Jens; Bučinská, Lenka Current Biology, Vol. 26, Issue 21 https://doi.org/10.1016/j.cub.2016.08.054	journal	November 2016
Characterization of Synechocystis sp. strain PCC 6803 and Δ nbl mutants under nitrogen-deficient conditions Li, Hong; Sherman, Louis Archives of Microbiology, Vol. 178, Issue 4 https://doi.org/10.1007/s00203-002-0446-y	journal	October 2002
When did oxygenic photosynthesis evolve? Buick, Roger Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504 https://doi.org/10.1098/rstb.2008.0041	journal	May 2008
Degradation of Phycobilisomes in Synechocystis sp. PCC6803 : EVIDENCE FOR ESSENTIAL FORMATION OF AN NblA1/NblA2 HETERODIMER AND ITS CODEGRADATION BY A Clp PROTEASE COMPLEX Baier, Antje; Winkler, Wiebke; Korte, Thomas Journal of Biological Chemistry, Vol. 289, Issue 17 https://doi.org/10.1074/jbc.M113.520601	journal	March 2014
nblS, a Gene Involved in Controlling Photosynthesis-Related Gene Expression during High Light and Nutrient Stress inSynechococcus elongatus PCC 7942 van Waasbergen, L. G.; Dolganov, N.; Grossman, A. R. Journal of Bacteriology, Vol. 184, Issue 9 https://doi.org/10.1128/JB.184.9.2481-2490.2002	journal	May 2002
In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells Vermaas, W. F. J.; Timlin, J. A.; Jones, H. D. T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10, p. 4050-4055 https://doi.org/10.1073/pnas.0708090105	journal	March 2008
Analysis of the self-shading effect on algal vertical distribution in natural waters Shigesada, Nanako; Okubo, Akira Journal of Mathematical Biology, Vol. 12, Issue 3 https://doi.org/10.1007/BF00276919	journal	August 1981
NblA1/A2-Dependent Homeostasis of Amino Acid Pools during Nitrogen Starvation in Synechocystis sp. PCC 6803 Kiyota, Hiroshi; Hirai, Masami; Ikeuchi, Masahiko Metabolites, Vol. 4, Issue 3 https://doi.org/10.3390/metabo4030517	journal	June 2014
The proteolysis adaptor, NblA, binds to the N-terminus of β-phycocyanin: Implications for the mechanism of phycobilisome degradation Nguyen, Amelia Y.; Bricker, William P.; Zhang, Hao Photosynthesis Research, Vol. 132, Issue 1 https://doi.org/10.1007/s11120-016-0334-y	journal	January 2017
Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival Gorl, M.; Sauer, J.; Baier, T. Microbiology, Vol. 144, Issue 9 https://doi.org/10.1099/00221287-144-9-2449	journal	September 1998
A simple viability analysis for unicellular cyanobacteria using a new autofluorescence assay, automated microscopy, and ImageJ Schulze, Katja; López, Diana A.; Tillich, Ulrich M. BMC Biotechnology, Vol. 11, Issue 1 https://doi.org/10.1186/1472-6750-11-118	journal	November 2011
Hyperspectral confocal microscope Sinclair, Michael B.; Haaland, David M.; Timlin, Jerilyn A. Applied Optics, Vol. 45, Issue 24, p. 6283-6291 https://doi.org/10.1364/AO.45.006283	journal	January 2006
Cyanobacterial Phycobilisomes MacColl, Robert Journal of Structural Biology, Vol. 124, Issue 2-3 https://doi.org/10.1006/jsbi.1998.4062	journal	December 1998
NblA, a Key Protein of Phycobilisome Degradation, Interacts with ClpC, a HSP100 Chaperone Partner of a Cyanobacterial Clp Protease Karradt, Anne; Sobanski, Johanna; Mattow, Jens Journal of Biological Chemistry, Vol. 283, Issue 47 https://doi.org/10.1074/jbc.M805823200	journal	September 2008
Phycobilisome: architecture of a light-harvesting supercomplex Watanabe, Mai; Ikeuchi, Masahiko Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9905-3	journal	October 2013
Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants Collins, Aaron M.; Liberton, Michelle; Jones, Howland D. T. Plant Physiology, Vol. 158, Issue 4 https://doi.org/10.1104/pp.111.192849	journal	February 2012
Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses Schwarz, R. Microbiology, Vol. 151, Issue 8 https://doi.org/10.1099/mic.0.27883-0	journal	August 2005
Assembly and Disassembly of Phycobilisomes Adir, Noam; Dines, Monica; Klartag, Merav Microbiology Monographs https://doi.org/10.1007/7171_020	book	January 2006
Phycobiliproteins and Complementary Chromatic Adaptation Bogorad, L. Annual Review of Plant Physiology, Vol. 26, Issue 1 https://doi.org/10.1146/annurev.pp.26.060175.002101	journal	June 1975
A Polypeptide with Similarity to Phycocyanin α-Subunit Phycocyanobilin Lyase Involved in Degradation of Phycobilisomes Dolganov, Nadia; Grossman, Arthur R. Journal of Bacteriology, Vol. 181, Issue 2 https://doi.org/10.1128/JB.181.2.610-617.1999	journal	January 1999
Assembly and Disassembly of Phycobilisomes Adir, Noam; Dines, Monica; Klartag, Merav Microbiology Monographs https://doi.org/10.1007/7171_020	book	January 2006
The proteolysis adaptor, NblA, binds to the N-terminus of β-phycocyanin: Implications for the mechanism of phycobilisome degradation Nguyen, Amelia Y.; Bricker, William P.; Zhang, Hao Photosynthesis Research, Vol. 132, Issue 1 https://doi.org/10.1007/s11120-016-0334-y	journal	January 2017
Photochemical activity and components of membrane preparations from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin Arnon, Daniel I.; McSwain, Berah D.; Tsujimoto, Harry Y. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 357, Issue 2 https://doi.org/10.1016/0005-2728(74)90063-2	journal	August 1974
Preprocessing strategies to improve MCR analyses of hyperspectral images Jones, Howland D.T.; Haaland, David M.; Sinclair, Michael B. Chemometrics and Intelligent Laboratory Systems, Vol. 117, p. 149-158 https://doi.org/10.1016/j.chemolab.2012.01.011	journal	August 2012
Awakening of a Dormant Cyanobacterium from Nitrogen Chlorosis Reveals a Genetically Determined Program Klotz, Alexander; Georg, Jens; Bučinská, Lenka Current Biology, Vol. 26, Issue 21 https://doi.org/10.1016/j.cub.2016.08.054	journal	November 2016
In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells Vermaas, W. F. J.; Timlin, J. A.; Jones, H. D. T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10, p. 4050-4055 https://doi.org/10.1073/pnas.0708090105	journal	March 2008
When did oxygenic photosynthesis evolve? Buick, Roger Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504 https://doi.org/10.1098/rstb.2008.0041	journal	May 2008
Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival Gorl, M.; Sauer, J.; Baier, T. Microbiology, Vol. 144, Issue 9 https://doi.org/10.1099/00221287-144-9-2449	journal	September 1998
Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses Schwarz, R. Microbiology, Vol. 151, Issue 8 https://doi.org/10.1099/mic.0.27883-0	journal	August 2005
Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants Collins, Aaron M.; Liberton, Michelle; Jones, Howland D. T. Plant Physiology, Vol. 158, Issue 4 https://doi.org/10.1104/pp.111.192849	journal	February 2012
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates Allen, Mary Mennes Journal of Phycology, Vol. 4, Issue 1 https://doi.org/10.1111/j.1529-8817.1968.tb04667.x	journal	March 1968
Expression of two nblA -homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803 Baier, Kerstin; Nicklisch, Sabine; Grundner, Christoph FEMS Microbiology Letters, Vol. 195, Issue 1 https://doi.org/10.1111/j.1574-6968.2001.tb10494.x	journal	February 2001
Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. Collier, J. L.; Grossman, A. R. Journal of Bacteriology, Vol. 174, Issue 14 https://doi.org/10.1128/jb.174.14.4718-4726.1992	journal	July 1992
Accuracy of extrapolated data as a function of prior knowledge and regularization Shieh, Hsin M.; Fiddy, Michael A. Applied Optics, Vol. 45, Issue 14 https://doi.org/10.1364/ao.45.003283	journal	May 2006

Cited By (5)

Cellular localization of tolyporphins, unusual tetrapyrroles, in a microbial photosynthetic community determined using hyperspectral confocal fluorescence microscopy Barnhart-Dailey, Meghan; Zhang, Yunlong; Zhang, Ran Photosynthesis Research, Vol. 141, Issue 3 https://doi.org/10.1007/s11120-019-00625-w	journal	March 2019
Distinct molecular signatures in dissolved organic matter produced by viral lysis of marine cyanobacteria: Molecular signatures of viral DOM release Ma, Xiufeng; Coleman, Maureen L.; Waldbauer, Jacob R. Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14338	journal	August 2018
Internalization and accumulation of model lignin breakdown products in bacteria and fungi Barnhart-Dailey, Meghan C.; Ye, Dongmei; Hayes, Dulce C. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1494-8	journal	July 2019
Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973 Nagarajan, Aparna; Zhou, Mowei; Nguyen, Amelia Y. Biomolecules, Vol. 9, Issue 8 https://doi.org/10.3390/biom9080374	journal	August 2019
Internalization and accumulation of model lignin breakdown products in bacteria and fungi Barnhart-Dailey, Meghan C.; Ye, Dongmei; Hayes, Dulce C. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1494-8	journal	July 2019

Similar Records

Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

Journal Article · 2017 · Plant Cell · OSTI ID:1670238

MacGregor-Chatwin, Craig; Sener, Melih; Barnett, Samuel F. H.; +7 more

Molecular Mechanism of Photoactivation and Structural Location of the Cyanobacterial Orange Carotenoid Protein

Journal Article · 2013 · Biochemistry · OSTI ID:1111577

Zhang, Hao; Liu, Haijun; Niedzwiedzki, Dariusz M.; +4 more

Organization and Flexibility of Cyanobacterial Thylakoid Membranes Examined by Neutron Scattering

Journal Article · 2013 · Journal of Biological Chemistry · OSTI ID:1059289

Liberton, Michelle; Page, Lawrence E.; O'Dell, William B.; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
Cyanobacteria
Photosynthesis
Phycobilisome
Nitrogen
Hyperspectral confocal fluorescence microscopy
Multivariate analysis

Title: Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels

Citation Formats

References (42)

Cited By (5)

Similar Records

Related Subjects