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

Abstract

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.

Authors:

Murton, Jaclyn;

;

; Liberton, Michelle;

;

Publication Date:: Fri Jul 21 00:00:00 EDT 2017

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

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1372115

Alternate Identifier(s):: OSTI ID: 1374747

Report Number(s):: SAND-2017-7775J
Journal ID: ISSN 0166-8595; PII: 422

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

Resource Type:: Published Article

Journal Name:: Photosynthesis Research

Additional Journal Information:: Journal Name: Photosynthesis Research; Journal ID: ISSN 0166-8595

Publisher:: Springer

Country of Publication:: Netherlands

Language:: English

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

Citation Formats


                    Murton, Jaclyn, Nagarajan, Aparna, Nguyen, Amelia Y., Liberton, Michelle, Hancock, Harmony A., Pakrasi, Himadri B., and Timlin, Jerilyn A. Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels.  Netherlands: N. p., 2017. 
Web.  doi:10.1007/s11120-017-0422-7.

Copy to clipboard


                    Murton, Jaclyn, Nagarajan, Aparna, Nguyen, Amelia Y., Liberton, Michelle, Hancock, Harmony A., Pakrasi, Himadri B., & Timlin, Jerilyn A. Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels.  Netherlands.  https://doi.org/10.1007/s11120-017-0422-7

Copy to clipboard


                    Murton, Jaclyn, Nagarajan, Aparna, Nguyen, Amelia Y., Liberton, Michelle, Hancock, Harmony A., Pakrasi, Himadri B., and Timlin, Jerilyn A. Fri .  
"Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels".  Netherlands.  https://doi.org/10.1007/s11120-017-0422-7.

Copy to clipboard


                    
@article{osti_1372115,

  title        = {Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels},

  author       = {Murton, Jaclyn and Nagarajan, Aparna and Nguyen, Amelia Y. and Liberton, Michelle and Hancock, Harmony A. and Pakrasi, Himadri B. and Timlin, Jerilyn A.},

  abstractNote = {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.},

  doi          = {10.1007/s11120-017-0422-7},

  journal      = {Photosynthesis Research},

  number       = ,

  volume       = ,

  place        = {Netherlands},

  year         = {Fri Jul 21 00:00:00 EDT 2017},

  month        = {Fri Jul 21 00:00:00 EDT 2017}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Publisher's Version of Record
https://doi.org/10.1007/s11120-017-0422-7

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 15 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referenced in this record:

A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria.
journal, March 1994

Collier, J. L.; Grossman, A. R.
The EMBO Journal, Vol. 13, Issue 5
DOI: 10.1002/j.1460-2075.1994.tb06352.x

Global Proteomics Reveal an Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations
journal, September 2010

Wegener, Kimberly M.; Singh, Abhay K.; Jacobs, Jon M.
Molecular & Cellular Proteomics, Vol. 9, Issue 12
DOI: 10.1074/mcp.M110.000109

A Polypeptide with Similarity to Phycocyanin α-Subunit Phycocyanobilin Lyase Involved in Degradation of Phycobilisomes
journal, January 1999

Dolganov, Nadia; Grossman, Arthur R.
Journal of Bacteriology, Vol. 181, Issue 2
DOI: 10.1128/JB.181.2.610-617.1999

Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
journal, March 1968

Allen, Mary Mennes
Journal of Phycology, Vol. 4, Issue 1
DOI: 10.1111/j.1529-8817.1968.tb04667.x

Expression of two nblA -homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803
journal, February 2001

Baier, Kerstin; Nicklisch, Sabine; Grundner, Christoph
FEMS Microbiology Letters, Vol. 195, Issue 1
DOI: 10.1111/j.1574-6968.2001.tb10494.x

Preprocessing strategies to improve MCR analyses of hyperspectral images
journal, August 2012

Jones, Howland D.T.; Haaland, David M.; Sinclair, Michael B.
Chemometrics and Intelligent Laboratory Systems, Vol. 117, p. 149-158
DOI: 10.1016/j.chemolab.2012.01.011

Tracking the Light Environment by Cyanobacteria and the Dynamic Nature of Light Harvesting
journal, February 2001

Grossman, Arthur R.; Bhaya, Devaki; He, Qingfang
Journal of Biological Chemistry, Vol. 276, Issue 15
DOI: 10.1074/jbc.R100003200

Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same.
journal, July 1992

Collier, J. L.; Grossman, A. R.
Journal of Bacteriology, Vol. 174, Issue 14
DOI: 10.1128/jb.174.14.4718-4726.1992

Awakening of a Dormant Cyanobacterium from Nitrogen Chlorosis Reveals a Genetically Determined Program
journal, November 2016

Klotz, Alexander; Georg, Jens; Bučinská, Lenka
Current Biology, Vol. 26, Issue 21
DOI: 10.1016/j.cub.2016.08.054

Characterization of Synechocystis sp. strain PCC 6803 and Δ nbl mutants under nitrogen-deficient conditions
journal, October 2002

Li, Hong; Sherman, Louis
Archives of Microbiology, Vol. 178, Issue 4
DOI: 10.1007/s00203-002-0446-y

When did oxygenic photosynthesis evolve?
journal, May 2008

Buick, Roger
Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504
DOI: 10.1098/rstb.2008.0041

Degradation of Phycobilisomes in Synechocystis sp. PCC6803 : EVIDENCE FOR ESSENTIAL FORMATION OF AN NblA1/NblA2 HETERODIMER AND ITS CODEGRADATION BY A Clp PROTEASE COMPLEX
journal, March 2014

Baier, Antje; Winkler, Wiebke; Korte, Thomas
Journal of Biological Chemistry, Vol. 289, Issue 17
DOI: 10.1074/jbc.M113.520601

nblS, a Gene Involved in Controlling Photosynthesis-Related Gene Expression during High Light and Nutrient Stress inSynechococcus elongatus PCC 7942
journal, May 2002

van Waasbergen, L. G.; Dolganov, N.; Grossman, A. R.
Journal of Bacteriology, Vol. 184, Issue 9
DOI: 10.1128/JB.184.9.2481-2490.2002

In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells
journal, March 2008

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
DOI: 10.1073/pnas.0708090105

Analysis of the self-shading effect on algal vertical distribution in natural waters
journal, August 1981

Shigesada, Nanako; Okubo, Akira
Journal of Mathematical Biology, Vol. 12, Issue 3
DOI: 10.1007/BF00276919

NblA1/A2-Dependent Homeostasis of Amino Acid Pools during Nitrogen Starvation in Synechocystis sp. PCC 6803
journal, June 2014

Kiyota, Hiroshi; Hirai, Masami; Ikeuchi, Masahiko
Metabolites, Vol. 4, Issue 3
DOI: 10.3390/metabo4030517

The proteolysis adaptor, NblA, binds to the N-terminus of β-phycocyanin: Implications for the mechanism of phycobilisome degradation
journal, January 2017

Nguyen, Amelia Y.; Bricker, William P.; Zhang, Hao
Photosynthesis Research, Vol. 132, Issue 1
DOI: 10.1007/s11120-016-0334-y

Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival
journal, September 1998

Gorl, M.; Sauer, J.; Baier, T.
Microbiology, Vol. 144, Issue 9
DOI: 10.1099/00221287-144-9-2449

A simple viability analysis for unicellular cyanobacteria using a new autofluorescence assay, automated microscopy, and ImageJ
journal, November 2011

Schulze, Katja; López, Diana A.; Tillich, Ulrich M.
BMC Biotechnology, Vol. 11, Issue 1
DOI: 10.1186/1472-6750-11-118

Hyperspectral confocal microscope
journal, January 2006

Sinclair, Michael B.; Haaland, David M.; Timlin, Jerilyn A.
Applied Optics, Vol. 45, Issue 24, p. 6283-6291
DOI: 10.1364/AO.45.006283

Cyanobacterial Phycobilisomes
journal, December 1998

MacColl, Robert
Journal of Structural Biology, Vol. 124, Issue 2-3
DOI: 10.1006/jsbi.1998.4062

NblA, a Key Protein of Phycobilisome Degradation, Interacts with ClpC, a HSP100 Chaperone Partner of a Cyanobacterial Clp Protease
journal, September 2008

Karradt, Anne; Sobanski, Johanna; Mattow, Jens
Journal of Biological Chemistry, Vol. 283, Issue 47
DOI: 10.1074/jbc.M805823200

Phycobilisome: architecture of a light-harvesting supercomplex
journal, October 2013

Watanabe, Mai; Ikeuchi, Masahiko
Photosynthesis Research, Vol. 116, Issue 2-3
DOI: 10.1007/s11120-013-9905-3

Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants
journal, February 2012

Collins, Aaron M.; Liberton, Michelle; Jones, Howland D. T.
Plant Physiology, Vol. 158, Issue 4
DOI: 10.1104/pp.111.192849

Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses
journal, August 2005

Schwarz, R.
Microbiology, Vol. 151, Issue 8
DOI: 10.1099/mic.0.27883-0

Assembly and Disassembly of Phycobilisomes
book, January 2006

Adir, Noam; Dines, Monica; Klartag, Merav
Microbiology Monographs
DOI: 10.1007/7171_020

Phycobiliproteins and Complementary Chromatic Adaptation
journal, June 1975

Bogorad, L.
Annual Review of Plant Physiology, Vol. 26, Issue 1
DOI: 10.1146/annurev.pp.26.060175.002101

Similar Records in DOE PAGES and OSTI.GOV collections:

Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

Journal Article MacGregor-Chatwin, Craig ; Sener, Melih ; Barnett, Samuel F. H. ; ... - The Plant Cell

Photosystem I (PSI) is the dominant photosystem in cyanobacteria and it plays a pivotal role in cyanobacterial metabolism. Despite its biological importance, the native organization of PSI in cyanobacterial thylakoid membranes is poorly understood. Here, we use atomic force microscopy (AFM) to show that ordered, extensive macromolecular arrays of PSI complexes are present in thylakoids from Thermosynechococcus elongatus, Synechococcus sp PCC 7002, and Synechocystis sp PCC 6803. Hyperspectral confocal fluorescence microscopy and three-dimensional structured illumination microscopy of Synechocystis sp PCC 6803 cells visualize PSI domains within the context of the complete thylakoid system. Crystallographic and AFM data were used tomore »« less
Cited by 48
https://doi.org/10.1105/tpc.17.00071
Molecular Mechanism of Photoactivation and Structural Location of the Cyanobacterial Orange Carotenoid Protein

Journal Article Zhang, Hao ; Liu, Haijun ; Niedzwiedzki, Dariusz M. ; ... - Biochemistry

The orange carotenoid protein (OCP) plays a photoprotective role in cyanobacterial photosynthesis similar to that of nonphotochemical quenching in higher plants. Under high-light conditions, the OCP binds to the phycobilisome (PBS) and reduces the extent of transfer of energy to the photosystems. The protective cycle starts from a light-induced activation of the OCP. Detailed information about the molecular mechanism of this process as well as the subsequent recruitment of the active OCP to the phycobilisome are not known. We report here our investigation on the OCP photoactivation from the cyanobacterium Synechocystis sp. PCC 6803 by using a combination of nativemore »« less
Cited by 80
https://doi.org/10.1021/bi401539w

Full Text Available
Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage

Journal Article Carrieri, Damian ; Lombardi, Thomas ; Paddock, Troy ; ... - Algal Research

Molecular mechanisms that regulate carbon flux are poorly understood in algae. The ΔglgC mutant of the cyanobacterium Synechocystis sp. PCC 6803 is incapable of glycogen storage and displays an array of physiological responses under nitrogen starvation that are different from wild-type (WT). These include non-bleaching phenotype and the redirection of photosynthetically fixed carbon towards excreted organic acids (overflow metabolism) without biomass growth. To understand the role of gene/protein expression in these responses, we followed the time course of transcripts by genome-scale microarrays and proteins by shotgun proteomics in ΔglgC and WT cells upon nitrogen starvation. Compared to WT, the degradationmore »« less
Cited by 17
https://doi.org/10.1016/j.algal.2016.11.003

Full Text Available
Subcellular pigment distribution is altered under far-red light acclimation in cyanobacteria that contain chlorophyll $$\mathcal{f}$$

Journal Article Majumder, Erica L. -W. ; Wolf, Benjamin M. ; Liu, Haijun ; ... - Photosynthesis Research

Far-Red Light (FRL) acclimation is a process that has been observed in cyanobacteria and algae that can grow solely on light above 700 nm. The acclimation to FRL results in rearrangement and synthesis of new pigments and pigment-protein complexes. Here, cyanobacteria containing chlorophyllmore »« less
Cited by 12
https://doi.org/10.1007/s11120-017-0428-1

Full Text Available
A Novel Mode of Photoprotection Mediated by a Cysteine Residue in the Chlorophyll Protein IsiA

Journal Article Chen, Hui-Yuan Steven ; Niedzwiedzki, Dariusz M. ; Bandyopadhyay, Anindita ; ... - mBio

Oxygenic photosynthetic organisms have evolved a multitude of mechanisms for protection against high-light stress. IsiA, a chlorophyll a-binding cyanobacterial protein, serves as an accessory antenna complex for photosystem I. Intriguingly, IsiA can also function as an independent pigment protein complex in the thylakoid membrane and facilitate the dissipation of excess energy, providing photoprotection. The molecular basis of the IsiA-mediated excitation quenching mechanism remains poorly understood. In this study, we demonstrate that IsiA uses a novel cysteine-mediated process to quench excitation energy. The single cysteine in IsiA in the cyanobacterium Synechocystis sp. strain PCC 6803 was converted to a valine. Ultrafastmore »« less
https://doi.org/10.1128/mbio.03663-20

Full Text Available

Similar Records

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

Abstract

Citation Formats

A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. journal, March 1994

Global Proteomics Reveal an Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations journal, September 2010

A Polypeptide with Similarity to Phycocyanin α-Subunit Phycocyanobilin Lyase Involved in Degradation of Phycobilisomes journal, January 1999

Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates journal, March 1968

Expression of two nblA -homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803 journal, February 2001

Preprocessing strategies to improve MCR analyses of hyperspectral images journal, August 2012

Tracking the Light Environment by Cyanobacteria and the Dynamic Nature of Light Harvesting journal, February 2001

Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. journal, July 1992

Awakening of a Dormant Cyanobacterium from Nitrogen Chlorosis Reveals a Genetically Determined Program journal, November 2016

Characterization of Synechocystis sp. strain PCC 6803 and Δ nbl mutants under nitrogen-deficient conditions journal, October 2002

When did oxygenic photosynthesis evolve? 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 journal, March 2014

nblS, a Gene Involved in Controlling Photosynthesis-Related Gene Expression during High Light and Nutrient Stress inSynechococcus elongatus PCC 7942 journal, May 2002

In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells journal, March 2008

Analysis of the self-shading effect on algal vertical distribution in natural waters journal, August 1981

NblA1/A2-Dependent Homeostasis of Amino Acid Pools during Nitrogen Starvation in Synechocystis sp. PCC 6803 journal, June 2014

The proteolysis adaptor, NblA, binds to the N-terminus of β-phycocyanin: Implications for the mechanism of phycobilisome degradation journal, January 2017

Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival journal, September 1998

A simple viability analysis for unicellular cyanobacteria using a new autofluorescence assay, automated microscopy, and ImageJ journal, November 2011

Hyperspectral confocal microscope journal, January 2006

Cyanobacterial Phycobilisomes journal, December 1998

NblA, a Key Protein of Phycobilisome Degradation, Interacts with ClpC, a HSP100 Chaperone Partner of a Cyanobacterial Clp Protease journal, September 2008

Phycobilisome: architecture of a light-harvesting supercomplex journal, October 2013

Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants journal, February 2012

Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses journal, August 2005

Assembly and Disassembly of Phycobilisomes book, January 2006

Phycobiliproteins and Complementary Chromatic Adaptation journal, June 1975

A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria.
journal, March 1994

Global Proteomics Reveal an Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations
journal, September 2010

A Polypeptide with Similarity to Phycocyanin α-Subunit Phycocyanobilin Lyase Involved in Degradation of Phycobilisomes
journal, January 1999

Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
journal, March 1968

Expression of two nblA -homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803
journal, February 2001

Preprocessing strategies to improve MCR analyses of hyperspectral images
journal, August 2012

Tracking the Light Environment by Cyanobacteria and the Dynamic Nature of Light Harvesting
journal, February 2001

Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same.
journal, July 1992

Awakening of a Dormant Cyanobacterium from Nitrogen Chlorosis Reveals a Genetically Determined Program
journal, November 2016

Characterization of Synechocystis sp. strain PCC 6803 and Δ nbl mutants under nitrogen-deficient conditions
journal, October 2002

When did oxygenic photosynthesis evolve?
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
journal, March 2014

nblS, a Gene Involved in Controlling Photosynthesis-Related Gene Expression during High Light and Nutrient Stress inSynechococcus elongatus PCC 7942
journal, May 2002

In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells
journal, March 2008

Analysis of the self-shading effect on algal vertical distribution in natural waters
journal, August 1981

NblA1/A2-Dependent Homeostasis of Amino Acid Pools during Nitrogen Starvation in Synechocystis sp. PCC 6803
journal, June 2014

The proteolysis adaptor, NblA, binds to the N-terminus of β-phycocyanin: Implications for the mechanism of phycobilisome degradation
journal, January 2017

Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival
journal, September 1998

A simple viability analysis for unicellular cyanobacteria using a new autofluorescence assay, automated microscopy, and ImageJ
journal, November 2011

Hyperspectral confocal microscope
journal, January 2006

Cyanobacterial Phycobilisomes
journal, December 1998

NblA, a Key Protein of Phycobilisome Degradation, Interacts with ClpC, a HSP100 Chaperone Partner of a Cyanobacterial Clp Protease
journal, September 2008

Phycobilisome: architecture of a light-harvesting supercomplex
journal, October 2013

Photosynthetic Pigment Localization and Thylakoid Membrane Morphology Are Altered in Synechocystis 6803 Phycobilisome Mutants
journal, February 2012

Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses
journal, August 2005

Assembly and Disassembly of Phycobilisomes
book, January 2006

Phycobiliproteins and Complementary Chromatic Adaptation
journal, June 1975