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.; Liberton, Michelle; Kedia, Komal; Shi, Tujin; Piehowski, Paul; Shukla, Anil; Fillmore, Thomas L.; Nicora, Carrie; Smith, Richard D.; Koppenaal, David W.; Jacobs, Jon M.; Pakrasi, Himadri B.

doi:10.3390/biom9080374

Title: Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973

Abstract

Phycobilisomes (PBSs) are large (3–5 megadalton) pigment-protein complexes in cyanobacteria that associate with thylakoid membranes and harvest light primarily for photosystem II. PBSs consist of highly ordered assemblies of pigmented phycobiliproteins (PBPs) and linker proteins that can account for up to half of the soluble protein in cells. Cyanobacteria adjust to changing environmental conditions by modulating PBS size and number. In response to nutrient depletion such as nitrogen (N) deprivation, PBSs are degraded in an extensive, tightly controlled, and reversible process. In Synechococcus elongatus UTEX 2973, a fast-growing cyanobacterium with a doubling time of two hours, the process of PBS degradation is very rapid, with 80% of PBSs per cell degraded in six hours under optimal light and CO₂ conditions. Proteomic analysis during PBS degradation and re-synthesis revealed multiple proteoforms of PBPs with partially degraded phycocyanobilin (PCB) pigments. NblA, a small proteolysis adaptor essential for PBS degradation, was characterized and validated with targeted mass spectrometry. NblA levels rose from essentially 0 to 25,000 copies per cell within 30 min of N depletion, and correlated with the rate of decrease in phycocyanin (PC). Implications of this correlation on the overall mechanism of PBS degradation during N deprivation are discussed.

Authors:

Nagarajan, Aparna;

;

; Liberton, Michelle; Kedia, Komal; Shi, Tujin;

; Shukla, Anil; Fillmore, Thomas L.; Nicora, Carrie; Smith, Richard D.; Koppenaal, David W.; Jacobs, Jon M.;

Publication Date:: Fri Aug 16 00:00:00 EDT 2019

Research Org.:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Org.:: USDOE Office of Science (SC)

OSTI Identifier:: 1557873

Alternate Identifier(s):: OSTI ID: 1641191

Report Number(s):: PNNL-SA-146394
Journal ID: ISSN 2218-273X; BIOMHC; PII: biom9080374

Grant/Contract Number:: FG02-99ER20350; AC05-76RL01830

Resource Type:: Published Article

Journal Name:: Biomolecules

Additional Journal Information:: Journal Name: Biomolecules Journal Volume: 9 Journal Issue: 8; Journal ID: ISSN 2218-273X

Publisher:: MDPI

Country of Publication:: Switzerland

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Nagarajan, Aparna, Zhou, Mowei, Nguyen, Amelia Y., Liberton, Michelle, Kedia, Komal, Shi, Tujin, Piehowski, Paul, Shukla, Anil, Fillmore, Thomas L., Nicora, Carrie, Smith, Richard D., Koppenaal, David W., Jacobs, Jon M., and Pakrasi, Himadri B. Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973.  Switzerland: N. p., 2019. 
Web.  doi:10.3390/biom9080374.

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                    Nagarajan, Aparna, Zhou, Mowei, Nguyen, Amelia Y., Liberton, Michelle, Kedia, Komal, Shi, Tujin, Piehowski, Paul, Shukla, Anil, Fillmore, Thomas L., Nicora, Carrie, Smith, Richard D., Koppenaal, David W., Jacobs, Jon M., & Pakrasi, Himadri B. Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973.  Switzerland.  https://doi.org/10.3390/biom9080374

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                    Nagarajan, Aparna, Zhou, Mowei, Nguyen, Amelia Y., Liberton, Michelle, Kedia, Komal, Shi, Tujin, Piehowski, Paul, Shukla, Anil, Fillmore, Thomas L., Nicora, Carrie, Smith, Richard D., Koppenaal, David W., Jacobs, Jon M., and Pakrasi, Himadri B. Fri .  
"Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973".  Switzerland.  https://doi.org/10.3390/biom9080374.

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@article{osti_1557873,

  title        = {Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973},

  author       = {Nagarajan, Aparna and Zhou, Mowei and Nguyen, Amelia Y. and Liberton, Michelle and Kedia, Komal and Shi, Tujin and Piehowski, Paul and Shukla, Anil and Fillmore, Thomas L. and Nicora, Carrie and Smith, Richard D. and Koppenaal, David W. and Jacobs, Jon M. and Pakrasi, Himadri B.},

  abstractNote = {Phycobilisomes (PBSs) are large (3–5 megadalton) pigment-protein complexes in cyanobacteria that associate with thylakoid membranes and harvest light primarily for photosystem II. PBSs consist of highly ordered assemblies of pigmented phycobiliproteins (PBPs) and linker proteins that can account for up to half of the soluble protein in cells. Cyanobacteria adjust to changing environmental conditions by modulating PBS size and number. In response to nutrient depletion such as nitrogen (N) deprivation, PBSs are degraded in an extensive, tightly controlled, and reversible process. In Synechococcus elongatus UTEX 2973, a fast-growing cyanobacterium with a doubling time of two hours, the process of PBS degradation is very rapid, with 80% of PBSs per cell degraded in six hours under optimal light and CO2 conditions. Proteomic analysis during PBS degradation and re-synthesis revealed multiple proteoforms of PBPs with partially degraded phycocyanobilin (PCB) pigments. NblA, a small proteolysis adaptor essential for PBS degradation, was characterized and validated with targeted mass spectrometry. NblA levels rose from essentially 0 to 25,000 copies per cell within 30 min of N depletion, and correlated with the rate of decrease in phycocyanin (PC). Implications of this correlation on the overall mechanism of PBS degradation during N deprivation are discussed.},

  doi          = {10.3390/biom9080374},

  journal      = {Biomolecules},

  number       = 8,

  volume       = 9,

  place        = {Switzerland},

  year         = {Fri Aug 16 00:00:00 EDT 2019},

  month        = {Fri Aug 16 00:00:00 EDT 2019}

}

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Title: Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973

Abstract

Citation Formats

A photocleavable surfactant for top-down proteomics journal, April 2019

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

TopPIC: a software tool for top-down mass spectrometry-based proteoform identification and characterization journal, July 2016

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

Top-Down Quantitative Proteomics Identified Phosphorylation of Cardiac Troponin I as a Candidate Biomarker for Chronic Heart Failure journal, September 2011

Quantitative Proteomic Analysis of Histone Modifications journal, October 2014

The PRIDE database and related tools and resources in 2019: improving support for quantification data journal, November 2018

Crystal Structure of NblA from Anabaena sp. PCC 7120, a Small Protein Playing a Key Role in Phycobilisome Degradation journal, December 2005

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

Identification and Quantification of Proteoforms by Mass Spectrometry journal, May 2019

Targeted Quantification of Low ng/mL Level Proteins in Human Serum without Immunoaffinity Depletion journal, June 2013

Skyline: an open source document editor for creating and analyzing targeted proteomics experiments journal, February 2010

Light Harvesting in Anacystis nidulans Studied in Pigment Mutants journal, December 1980

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

Phosphoproteome of the cyanobacterium Synechocystis sp. PCC 6803 and its dynamics during nitrogen starvation journal, March 2015

Isobaric Labeling-Based Relative Quantification in Shotgun Proteomics journal, November 2014

Changes in the cyanobacterial photosynthetic apparatus during acclimation to macronutrient deprivation journal, December 1994

The c-di-GMP Binding Protein YcgR Controls Flagellar Motor Direction and Speed to Affect Chemotaxis by a “Backstop Brake” Mechanism journal, April 2010

Comparative genomics reveals the molecular determinants of rapid growth of the cyanobacterium Synechococcus elongatus UTEX 2973 journal, November 2018

Top-down characterization of endogenous protein complexes with native proteomics journal, November 2017

Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant journal, July 2005

Changes in polypeptide composition of Synechocystis sp. strain 6308 phycobilisomes induced by nitrogen starvation. journal, April 1989

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. Low-Level Photosynthesis As a Mechanism of Long-Term Survival journal, May 2001

Advancing the sensitivity of selected reaction monitoring-based targeted quantitative proteomics journal, April 2012

Informed-Proteomics: open-source software package for top-down proteomics journal, August 2017

CONSeQuence: Prediction of Reference Peptides for Absolute Quantitative Proteomics Using Consensus Machine Learning Approaches journal, August 2011

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

Phycobiliproteins and Complementary Chromatic Adaptation journal, June 1975

Progress in Top-Down Proteomics and the Analysis of Proteoforms journal, June 2016

Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ journal, June 2014

Chlorosis as a Developmental Program in Cyanobacteria: The Proteomic Fundament for Survival and Awakening journal, May 2018

Cyanobacterial high-light-inducible proteins — Protectors of chlorophyll–protein synthesis and assembly journal, March 2016

Nitrogen or Sulfur Starvation Differentially Affects Phycobilisome Degradation and Expression of the nblA Gene in Synechocystis Strain PCC 6803 journal, May 2001

Elucidating Escherichia coli Proteoform Families Using Intact-Mass Proteomics and a Global PTM Discovery Database journal, October 2017

Different roles for ApcD and ApcF in Synechococcus elongatus and Synechocystis sp. PCC 6803 phycobilisomes journal, June 2019

Applying Label-Free Quantitation to Top Down Proteomics journal, May 2014

Prediction of high-responding peptides for targeted protein assays by mass spectrometry journal, January 2009

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

Quantitative proteomics: challenges and opportunities in basic and applied research journal, June 2017

Origin of the F685 and F695 fluorescence in Photosystem II journal, June 2005

Structure of phycobilisome from the red alga Griffithsia pacifica journal, October 2017

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

Protein Identification Using Top-Down Spectra journal, October 2011

Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels journal, July 2017

Effects of Chlorophyll Availability on Phycobilisomes in Synechocystis sp. PCC 6803 journal, December 1999

Genetic analysis of a 9 kDa phycocyanin-associated linker polypeptide journal, August 1990

Phycobiliprotein methylation journal, August 1990

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 journal, August 1974

A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions journal, September 1998

Adjustments to Photosystem Stoichiometry and Electron Transfer Proteins Are Key to the Remarkably Fast Growth of the Cyanobacterium Synechococcus elongatus UTEX 2973 journal, February 2018

Synechococcus elongatus UTEX 2973, a fast growing cyanobacterial chassis for biosynthesis using light and CO2 journal, January 2015

Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane journal, April 2009

Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation journal, November 2018

Biogenesis of Phycobiliproteins journal, January 2008

A photocleavable surfactant for top-down proteomics
journal, April 2019

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

TopPIC: a software tool for top-down mass spectrometry-based proteoform identification and characterization
journal, July 2016

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

Top-Down Quantitative Proteomics Identified Phosphorylation of Cardiac Troponin I as a Candidate Biomarker for Chronic Heart Failure
journal, September 2011

Quantitative Proteomic Analysis of Histone Modifications
journal, October 2014

The PRIDE database and related tools and resources in 2019: improving support for quantification data
journal, November 2018

Crystal Structure of NblA from Anabaena sp. PCC 7120, a Small Protein Playing a Key Role in Phycobilisome Degradation
journal, December 2005

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

Identification and Quantification of Proteoforms by Mass Spectrometry
journal, May 2019

Targeted Quantification of Low ng/mL Level Proteins in Human Serum without Immunoaffinity Depletion
journal, June 2013

Skyline: an open source document editor for creating and analyzing targeted proteomics experiments
journal, February 2010

Light Harvesting in Anacystis nidulans Studied in Pigment Mutants
journal, December 1980

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

Phosphoproteome of the cyanobacterium Synechocystis sp. PCC 6803 and its dynamics during nitrogen starvation
journal, March 2015

Isobaric Labeling-Based Relative Quantification in Shotgun Proteomics
journal, November 2014

Changes in the cyanobacterial photosynthetic apparatus during acclimation to macronutrient deprivation
journal, December 1994

The c-di-GMP Binding Protein YcgR Controls Flagellar Motor Direction and Speed to Affect Chemotaxis by a “Backstop Brake” Mechanism
journal, April 2010

Comparative genomics reveals the molecular determinants of rapid growth of the cyanobacterium Synechococcus elongatus UTEX 2973
journal, November 2018

Top-down characterization of endogenous protein complexes with native proteomics
journal, November 2017

Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant
journal, July 2005

Changes in polypeptide composition of Synechocystis sp. strain 6308 phycobilisomes induced by nitrogen starvation.
journal, April 1989

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. Low-Level Photosynthesis As a Mechanism of Long-Term Survival
journal, May 2001

Advancing the sensitivity of selected reaction monitoring-based targeted quantitative proteomics
journal, April 2012

Informed-Proteomics: open-source software package for top-down proteomics
journal, August 2017

CONSeQuence: Prediction of Reference Peptides for Absolute Quantitative Proteomics Using Consensus Machine Learning Approaches
journal, August 2011

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

Phycobiliproteins and Complementary Chromatic Adaptation
journal, June 1975

Progress in Top-Down Proteomics and the Analysis of Proteoforms
journal, June 2016

Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ
journal, June 2014

Chlorosis as a Developmental Program in Cyanobacteria: The Proteomic Fundament for Survival and Awakening
journal, May 2018

Cyanobacterial high-light-inducible proteins — Protectors of chlorophyll–protein synthesis and assembly
journal, March 2016

Nitrogen or Sulfur Starvation Differentially Affects Phycobilisome Degradation and Expression of the nblA Gene in Synechocystis Strain PCC 6803
journal, May 2001

Elucidating Escherichia coli Proteoform Families Using Intact-Mass Proteomics and a Global PTM Discovery Database
journal, October 2017

Different roles for ApcD and ApcF in Synechococcus elongatus and Synechocystis sp. PCC 6803 phycobilisomes
journal, June 2019

Applying Label-Free Quantitation to Top Down Proteomics
journal, May 2014

Prediction of high-responding peptides for targeted protein assays by mass spectrometry
journal, January 2009

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

Quantitative proteomics: challenges and opportunities in basic and applied research
journal, June 2017

Origin of the F685 and F695 fluorescence in Photosystem II
journal, June 2005

Structure of phycobilisome from the red alga Griffithsia pacifica
journal, October 2017

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

Protein Identification Using Top-Down Spectra
journal, October 2011

Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels
journal, July 2017

Effects of Chlorophyll Availability on Phycobilisomes in Synechocystis sp. PCC 6803
journal, December 1999

Genetic analysis of a 9 kDa phycocyanin-associated linker polypeptide
journal, August 1990

Phycobiliprotein methylation
journal, August 1990

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
journal, August 1974

A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions
journal, September 1998

Adjustments to Photosystem Stoichiometry and Electron Transfer Proteins Are Key to the Remarkably Fast Growth of the Cyanobacterium Synechococcus elongatus UTEX 2973
journal, February 2018

Synechococcus elongatus UTEX 2973, a fast growing cyanobacterial chassis for biosynthesis using light and CO2
journal, January 2015

Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane
journal, April 2009

Nitrogen chlorosis in unicellular cyanobacteria – a developmental program for surviving nitrogen deprivation
journal, November 2018

Biogenesis of Phycobiliproteins
journal, January 2008