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:
- Publication Date:
- 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.
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
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.
@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 = {2017},
month = {7}
}
https://doi.org/10.1007/s11120-017-0422-7
Web of Science
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
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
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
journal, March 1968
- Allen, Mary Mennes
- Journal of Phycology, Vol. 4, Issue 1
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
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
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
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
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
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
When did oxygenic photosynthesis evolve?
journal, May 2008
- Buick, Roger
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504
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
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
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
Green Autofluorescence in Dinoflagellates, Diatoms, and Other Microalgae and Its Implications for Vital Staining and Morphological Studies
journal, February 2007
- Tang, Y. Z.; Dobbs, F. C.
- Applied and Environmental Microbiology, Vol. 73, Issue 7
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
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
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
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
Hyperspectral confocal microscope
journal, January 2006
- Sinclair, Michael B.; Haaland, David M.; Timlin, Jerilyn A.
- Applied Optics, Vol. 45, Issue 24, p. 6283-6291
Cyanobacterial Phycobilisomes
journal, December 1998
- MacColl, Robert
- Journal of Structural Biology, Vol. 124, Issue 2-3
Phycobilisome: architecture of a light-harvesting supercomplex
journal, October 2013
- Watanabe, Mai; Ikeuchi, Masahiko
- Photosynthesis Research, Vol. 116, Issue 2-3
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
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
Phycobiliproteins and Complementary Chromatic Adaptation
journal, June 1975
- Bogorad, L.
- Annual Review of Plant Physiology, Vol. 26, Issue 1
Works referencing / citing this record:
Cellular localization of tolyporphins, unusual tetrapyrroles, in a microbial photosynthetic community determined using hyperspectral confocal fluorescence microscopy
journal, March 2019
- Barnhart-Dailey, Meghan; Zhang, Yunlong; Zhang, Ran
- Photosynthesis Research, Vol. 141, Issue 3
Chlorosis as a Developmental Program in Cyanobacteria: The Proteomic Fundament for Survival and Awakening
journal, May 2018
- Spät, Philipp; Klotz, Alexander; Rexroth, Sascha
- Molecular & Cellular Proteomics, Vol. 17, Issue 9
Distinct molecular signatures in dissolved organic matter produced by viral lysis of marine cyanobacteria: Molecular signatures of viral DOM release
journal, August 2018
- Ma, Xiufeng; Coleman, Maureen L.; Waldbauer, Jacob R.
- Environmental Microbiology, Vol. 20, Issue 8
Internalization and accumulation of model lignin breakdown products in bacteria and fungi
journal, July 2019
- Barnhart-Dailey, Meghan C.; Ye, Dongmei; Hayes, Dulce C.
- Biotechnology for Biofuels, Vol. 12, Issue 1
Proteomic Insights into Phycobilisome Degradation, A Selective and Tightly Controlled Process in The Fast-Growing Cyanobacterium Synechococcus elongatus UTEX 2973
journal, August 2019
- Nagarajan, Aparna; Zhou, Mowei; Nguyen, Amelia Y.
- Biomolecules, Vol. 9, Issue 8