Coping with iron limitation: A metabolomic study of Synechocystis sp. PCC 6803

Rivas-Ubach, Albert; Poret-Peterson, Amisha T.; Peñuelas, Josep; Sardans, Jordi; Pérez-Trujillo, Míriam; Legido-Quigley, Cristina; Oravec, Michal; Urban, Otmar; Elser, James J.

doi:10.1007/s11738-018-2603-1

Title: Coping with iron limitation: A metabolomic study of Synechocystis sp. PCC 6803

Journal Article · Tue Jan 16 00:00:00 EST 2018 · Acta Physiologiae Plantarum

DOI:https://doi.org/10.1007/s11738-018-2603-1· OSTI ID:1439015

Rivas-Ubach, Albert; Poret-Peterson, Amisha T.; Peñuelas, Josep; Sardans, Jordi; Pérez-Trujillo, Míriam; Legido-Quigley, Cristina; Oravec, Michal; Urban, Otmar; Elser, James J.

Iron (Fe) is a key element for all living systems, especially for photosynthetic organisms because of its important role in the photosynthetic electron transport chain. Fe limitation in cyanobacteria leads to several physiological and morphological changes. However, the overall metabolic responses to Fe limitation are still poorly understood. In this study, we integrated elemental, stoichiometric, macromolecular, and metabolomic data to shed light on the responses of Synechocystis sp. PCC 6803, a non-N2-fixing freshwater cyanobacterium, to Fe limitation. Compared to Synechocystis growing at nutrient replete conditions, Fe-limited cultures had lower growth rates and amounts of chlorophyll a, RNA, RNA:DNA, C, N, and P and higher ratios of Protein:RNA, C:N, C:P and N:P, in accordance with the growth rate hypothesis which predicts faster growing organisms will have decreased biomass RNA contents and C:P and N:P ratios. Fe-limited Synechocystis had lower amounts Fe, Mn and Mo, and higher amount of Cu. Several changes in amino acids of cultures growing under Fe limitation suggest nitrogen limitation. Additionally, we found substantial increases in stress-related metabolites in Fe-limited cyanobacteria such antioxidants. This study represents an advance in understanding the stoichiometric, macromolecular and metabolic strategies that cyanobacteria use to cope with Fe limitation. This information, moreover, may further understanding of changes in cyanobacterial functions under scenarios of Fe limitation in aquatic ecosystems.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1439015

Report Number(s):: PNNL-SA-132877; KP1704020

Journal Information:: Acta Physiologiae Plantarum, Vol. 40, Issue 2; ISSN 0137-5881

Country of Publication:: United States

Language:: English

References (72)

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
Negative impact of nitrogen deposition on soil buffering capacity Bowman, William D.; Cleveland, Cory C.; Halada, Ĺuboš Nature Geoscience, Vol. 1, Issue 11 https://doi.org/10.1038/ngeo339	journal	November 2008
Evidence for a role for L-proline as a salinity protectant in the cyanobacterium Nostoc muscorum Singh, A. K.; Chakravarthy, D.; Singh, T. P. K. Plant, Cell and Environment, Vol. 19, Issue 4 https://doi.org/10.1111/j.1365-3040.1996.tb00342.x	journal	April 1996
Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes? Rivas-Ubach, Albert; Hódar, José A.; Sardans, Jordi Ecology and Evolution, Vol. 6, Issue 13 https://doi.org/10.1002/ece3.2206	journal	June 2016
Metabolomics and its use in ecology: Metabolomics in Ecology Jones, Oliver A. H.; Maguire, Mahon L.; Griffin, Julian L. Austral Ecology, Vol. 38, Issue 6 https://doi.org/10.1111/aec.12019	journal	January 2013
Bacterial respiration: a flexible process for a changing environment Richardson, David J. Microbiology, Vol. 146, Issue 3 https://doi.org/10.1099/00221287-146-3-551	journal	March 2000
Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions Shi, D.; Kranz, S. A.; Kim, J. -M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 45 https://doi.org/10.1073/pnas.1216012109	journal	October 2012
Photophysiological Expressions of Iron Stress in Phytoplankton Behrenfeld, Michael J.; Milligan, Allen J. Annual Review of Marine Science, Vol. 5, Issue 1 https://doi.org/10.1146/annurev-marine-121211-172356	journal	January 2013
An LC–MS-Based Chemical and Analytical Method for Targeted Metabolite Quantification in the Model Cyanobacterium Synechococcus sp. PCC 7002 Bennette, Nicholas B.; Eng, John F.; Dismukes, G. Charles Analytical Chemistry, Vol. 83, Issue 10 https://doi.org/10.1021/ac200108a	journal	May 2011
Iron deprivation in cyanobacteria Ferreira, Fernando; Straus, Neil A. Journal of Applied Phycology, Vol. 6, Issue 2 https://doi.org/10.1007/BF02186073	journal	April 1994
Strong relationship between elemental stoichiometry and metabolome in plants Rivas-Ubach, A.; Sardans, J.; Perez-Trujillo, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1116092109	journal	February 2012
Organism Size, Life History, and N:P Stoichiometry Elser, James J.; Dobberfuhl, Dean R.; MacKay, Neil A. BioScience, Vol. 46, Issue 9 https://doi.org/10.2307/1312897	journal	October 1996
Characterization of the natural variation in Arabidopsis thaliana metabolome by the analysis of metabolic distance Houshyani, Benyamin; Kabouw, Patrick; Muth, Dorota Metabolomics, Vol. 8, Issue S1 https://doi.org/10.1007/s11306-011-0375-3	journal	October 2011
A trace metal clean reagent to remove surface-bound iron from marine phytoplankton Tovar-Sanchez, Antonio; Sañudo-Wilhelmy, Sergio A.; Garcia-Vargas, Manuel Marine Chemistry, Vol. 82, Issue 1-2 https://doi.org/10.1016/S0304-4203(03)00054-9	journal	June 2003
Comparative Analysis of the Primary Transcriptome of Synechocystis sp. PCC 6803 Kopf, Matthias; Klähn, Stephan; Scholz, Ingeborg DNA Research, Vol. 21, Issue 5 https://doi.org/10.1093/dnares/dsu018	journal	June 2014
Widespread Iron Limitation of Phytoplankton in the South Pacific Ocean Behrenfeld, M. J. Science, Vol. 283, Issue 5403 https://doi.org/10.1126/science.283.5403.840	journal	February 1999
Proteomic analyses of the response of cyanobacteria to different stress conditions Castielli, Ornella; De la Cerda, Berta; Navarro, José A. FEBS Letters, Vol. 583, Issue 11 https://doi.org/10.1016/j.febslet.2009.03.069	journal	April 2009
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-395	journal	July 2010
Photosynthetic nitrate assimilation in cyanobacteria Flores, Enrique; Frías, José E.; Rubio, Luis M. Photosynthesis Research, Vol. 83, Issue 2 https://doi.org/10.1007/s11120-004-5830-9	journal	February 2005
Iron-Binding Activity of FutA1 Subunit of an ABC-type Iron Transporter in the Cyanobacterium Synechocystis sp. Strain PCC 6803 Katoh, Hirokazu; Hagino, Natsu; Ogawa, Teruo Plant and Cell Physiology, Vol. 42, Issue 8 https://doi.org/10.1093/pcp/pce106	journal	August 2001
Critical Roles of Bacterioferritins in Iron Storage and Proliferation of Cyanobacteria Keren, Nir; Aurora, Rajeev; Pakrasi, Himadri B. Plant Physiology, Vol. 135, Issue 3 https://doi.org/10.1104/pp.104.042770	journal	July 2004
Tocopherols Protect Synechocystis sp. Strain PCC 6803 from Lipid Peroxidation Maeda, Hiroshi; Sakuragi, Yumiko; Bryant, Donald A. Plant Physiology, Vol. 138, Issue 3 https://doi.org/10.1104/pp.105.061135	journal	June 2005
Characteristics of the Freshwater Cyanobacterium Microcystis aeruginosa Grown in Iron-Limited Continuous Culture Dang, T. C.; Fujii, M.; Rose, A. L. Applied and Environmental Microbiology, Vol. 78, Issue 5 https://doi.org/10.1128/AEM.06908-11	journal	December 2011
Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean Behrenfeld, Michael J.; Bale, Anthony J.; Kolber, Zbigniew S. Nature, Vol. 383, Issue 6600 https://doi.org/10.1038/383508a0	journal	October 1996
THE CYANOBACTERIAL CHLOROPHYLL-BINDING-PROTEIN ISIA ACTS TO INCREASE THE IN VIVO EFFECTIVE ABSORPTION CROSS-SECTION OF PSI UNDER IRON LIMITATION1: IsiA INCREASES THE IN VIVO ABSORPTION CROSS-SECTION OF PSI Ryan-Keogh, Thomas J.; Macey, Anna I.; Cockshutt, Amanda M. Journal of Phycology, Vol. 48, Issue 1 https://doi.org/10.1111/j.1529-8817.2011.01092.x	journal	December 2011
The role of trace metals in photosynthetic electron transport in O₂-evolving organisms Raven, John A.; Evans, Michael C. W.; Korb, Rebecca E. Photosynthesis Research, Vol. 60, Issue 2/3, p. 111-150 https://doi.org/10.1023/A:1006282714942	journal	January 1999
Genes Essential to Iron Transport in the Cyanobacterium Synechocystis sp. Strain PCC 6803 Katoh, H.; Hagino, N.; Grossman, A. R. Journal of Bacteriology, Vol. 183, Issue 9 https://doi.org/10.1128/JB.183.9.2779-2784.2001	journal	May 2001
Genomic perspectives in microbial oceanography DeLong, Edward F.; Karl, David M. Nature, Vol. 437, Issue 7057 https://doi.org/10.1038/nature04157	journal	September 2005
Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation Mackey, Katherine R. M.; Post, Anton F.; McIlvin, Matthew R. Proceedings of the National Academy of Sciences, Vol. 112, Issue 32 https://doi.org/10.1073/pnas.1509448112	journal	July 2015
LC–MS metabolic profiling of Arabidopsis thaliana plant leaves and cell cultures: Optimization of pre-LC–MS procedure parameters t’Kindt, Ruben; De Veylder, Lieven; Storme, Michael Journal of Chromatography B, Vol. 871, Issue 1 https://doi.org/10.1016/j.jchromb.2008.06.039	journal	August 2008
Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803 Grundel, M.; Scheunemann, R.; Lockau, W. Microbiology, Vol. 158, Issue Pt_12 https://doi.org/10.1099/mic.0.062950-0	journal	October 2012
Molecular biology of cyanobacterial salt acclimation Hagemann, Martin FEMS Microbiology Reviews, Vol. 35, Issue 1 https://doi.org/10.1111/j.1574-6976.2010.00234.x	journal	January 2011
Metal Homeostasis in Cyanobacteria and Chloroplasts. Balancing Benefits and Risks to the Photosynthetic Apparatus Shcolnick, Sigal; Keren, Nir Plant Physiology, Vol. 141, Issue 3 https://doi.org/10.1104/pp.106.079251	journal	July 2006
Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion Hasunuma, Tomohisa; Kikuyama, Fumi; Matsuda, Mami Journal of Experimental Botany, Vol. 64, Issue 10 https://doi.org/10.1093/jxb/ert134	journal	May 2013
An eco-metabolomic study of host plant resistance to Western flower thrips in cultivated, biofortified and wild carrots Leiss, Kirsten A.; Cristofori, Gabriele; van Steenis, Rosalinda Phytochemistry, Vol. 93 https://doi.org/10.1016/j.phytochem.2013.03.011	journal	September 2013
Flux Balance Analysis of Cyanobacterial Metabolism: The Metabolic Network of Synechocystis sp. PCC 6803 Knoop, Henning; Gründel, Marianne; Zilliges, Yvonne PLoS Computational Biology, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pcbi.1003081	journal	June 2013
Observing and interpreting correlations in metabolomic networks Steuer, R.; Kurths, J.; Fiehn, O. Bioinformatics, Vol. 19, Issue 8 https://doi.org/10.1093/bioinformatics/btg120	journal	May 2003
Metabolomics – the link between genotypes and phenotypes Fiehn, Oliver Plant Molecular Biology, Vol. 48, Issue 1/2, p. 155-171 https://doi.org/10.1023/A:1013713905833	journal	January 2002
Modulation of the Major Paths of Carbon in Photorespiratory Mutants of Synechocystis Huege, Jan; Goetze, Jan; Schwarz, Doreen PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016278	journal	January 2011
Biological stoichiometry from genes to ecosystems Elser, J. J.; Sterner, R. W.; Gorokhova, E. Ecology Letters, Vol. 3, Issue 6 https://doi.org/10.1111/j.1461-0248.2000.00185.x	journal	November 2000
Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803 Singh, Abhay K.; Li, Hong; Sherman, Louis A. Physiologia Plantarum, Vol. 120, Issue 1 https://doi.org/10.1111/j.0031-9317.2004.0232.x	journal	January 2004
Metabolomics: the chemistry between ecology and genetics: INVITED TECHNICAL REVIEW Macel, Mirka; Van DAM, Nicole M.; Keurentjes, Joost J. B. Molecular Ecology Resources, Vol. 10, Issue 4 https://doi.org/10.1111/j.1755-0998.2010.02854.x	journal	March 2010
Capillary electrophoresis-mass spectrometry reveals the distribution of carbon metabolites during nitrogen starvation in Synechocystis sp. PCC 6803 : Carbon distribution in N-starved Osanai, Takashi; Oikawa, Akira; Shirai, Tomokazu Environmental Microbiology, Vol. 16, Issue 2 https://doi.org/10.1111/1462-2920.12170	journal	June 2013
Similar local, but different systemic, metabolomic responses of closely related pine subspecies to folivory by caterpillars of the processionary moth Rivas-Ubach, A.; Sardans, J.; Hódar, J. A. Plant Biology, Vol. 18, Issue 3 https://doi.org/10.1111/plb.12422	journal	December 2015
Topsoil depth substantially influences the responses to drought of the foliar metabolomes of Mediterranean forests Rivas-Ubach, Albert; Barbeta, Adrià; Sardans, Jordi Perspectives in Plant Ecology, Evolution and Systematics, Vol. 21 https://doi.org/10.1016/j.ppees.2016.06.001	journal	August 2016
Coordinated transporter activity shapes high-affinity iron acquisition in cyanobacteria Kranzler, Chana; Lis, Hagar; Finkel, Omri M. The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.161	journal	October 2013
Structure-Function of the Cytochrome b ₆ f Complex ^† Baniulis, D.; Yamashita, E.; Zhang, H. Photochemistry and Photobiology, Vol. 84, Issue 6 https://doi.org/10.1111/j.1751-1097.2008.00444.x	journal	November 2008
Iron Deprivation in Synechocystis : Inference of Pathways, Non-coding RNAs, and Regulatory Elements from Comprehensive Expression Profiling Hernández-Prieto, Miguel A.; Schön, Verena; Georg, Jens G3: Genes\|Genomes\|Genetics, Vol. 2, Issue 12 https://doi.org/10.1534/g3.112.003863	journal	December 2012
Ecometabolomics: optimized NMR-based method Rivas-Ubach, Albert; Pérez-Trujillo, Miriam; Sardans, Jordi Methods in Ecology and Evolution, Vol. 4, Issue 5 https://doi.org/10.1111/2041-210X.12028	journal	February 2013
Essential metals for nitrogen fixation in a free-living N ₂ -fixing bacterium: chelation, homeostasis and high use efficiency : Homeostasis of nitrogenase metal cofactors in Bellenger, J. -P.; Wichard, T.; Xu, Y. Environmental Microbiology, Vol. 13, Issue 6 https://doi.org/10.1111/j.1462-2920.2011.02440.x	journal	March 2011
The hierarchy of transition metal homeostasis: Iron controls manganese accumulation in a unicellular cyanobacterium Sharon, Shir; Salomon, Eitan; Kranzler, Chana Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 12 https://doi.org/10.1016/j.bbabio.2014.09.007	journal	December 2014
Close and distant: Contrasting the metabolism of two closely related subspecies of Scots pine under the effects of folivory and summer drought Rivas-Ubach, Albert; Sardans, Jordi; Hódar, José Antonio Ecology and Evolution, Vol. 7, Issue 21 https://doi.org/10.1002/ece3.3343	journal	September 2017
The Mechanism of Iron Homeostasis in the Unicellular Cyanobacterium Synechocystis sp. PCC 6803 and Its Relationship to Oxidative Stress Shcolnick, Sigal; Summerfield, Tina C.; Reytman, Lilia Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.141853	journal	June 2009
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
A Two-component Signal Transduction Pathway Regulates Manganese Homeostasis in Synechocystis 6803, a Photosynthetic Organism Ogawa, Teruo; Bao, Ding Hui; Katoh, Hirokazu Journal of Biological Chemistry, Vol. 277, Issue 32 https://doi.org/10.1074/jbc.M204175200	journal	May 2002
Ecological metabolomics Peñuelas, Josep; Sardans, Jordi Chemistry and Ecology, Vol. 25, Issue 4 https://doi.org/10.1080/02757540903062517	journal	August 2009
Succinate Dehydrogenase and Other Respiratory Pathways in Thylakoid Membranes of Synechocystis sp. Strain PCC 6803: Capacity Comparisons and Physiological Function Cooley, J. W.; Vermaas, W. F. J. Journal of Bacteriology, Vol. 183, Issue 14 https://doi.org/10.1128/JB.183.14.4251-4258.2001	journal	July 2001
Copper(II), nickel(II), zinc(II), and molybdenum(VI) complexes of desferrioxamine B in aqueous solution Farkas, Etelka; Csóka, Hajnalka; Micera, Giovanni Journal of Inorganic Biochemistry, Vol. 65, Issue 4 https://doi.org/10.1016/S0162-0134(96)00144-4	journal	March 1997
Phytochemical composition of Potentilla anserina L. analyzed by an integrative GC-MS and LC-MS metabolomics platform Mari, Angela; Lyon, David; Fragner, Lena Metabolomics, Vol. 9, Issue 3 https://doi.org/10.1007/s11306-012-0473-x	journal	November 2012
Effect of Ocean Acidification on Iron Availability to Marine Phytoplankton Shi, D.; Xu, Y.; Hopkinson, B. M. Science, Vol. 327, Issue 5966 https://doi.org/10.1126/science.1183517	journal	January 2010
Proline: a multifunctional amino acid Szabados, László; Savouré, Arnould Trends in Plant Science, Vol. 15, Issue 2 https://doi.org/10.1016/j.tplants.2009.11.009	journal	February 2010
Opposite metabolic responses of shoots and roots to drought Gargallo-Garriga, Albert; Sardans, Jordi; Pérez-Trujillo, Míriam Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06829	journal	October 2014
Drought enhances folivory by shifting foliar metabolomes in Quercus ilex trees Rivas-Ubach, Albert; Gargallo-Garriga, Albert; Sardans, Jordi New Phytologist, Vol. 202, Issue 3 https://doi.org/10.1111/nph.12687	journal	January 2014
Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots Gargallo-Garriga, Albert; Sardans, Jordi; Pérez-Trujillo, Míriam New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13377	journal	March 2015
Metabolomic Response of Chlamydomonas reinhardtii to the Inhibition of Target of Rapamycin (TOR) by Rapamycin Lee, Do Yup Journal of Microbiology and Biotechnology, Vol. 23, Issue 7 https://doi.org/10.4014/jmb.1304.04057	journal	July 2013
Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria Bibby, Thomas S.; Nield, Jon; Barber, James Nature, Vol. 412, Issue 6848 https://doi.org/10.1038/35089098	journal	August 2001
Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC6803. II. Sequence Determination of the Entire Genome and Assignment of Potential Protein-coding Regions Kaneko, T.; Sato, S.; Kotani, H. DNA Research, Vol. 3, Issue 3 https://doi.org/10.1093/dnares/3.3.109	journal	January 1996
Oxidative stress in cyanobacteria Latifi, Amel; Ruiz, Marion; Zhang, Cheng-Cai FEMS Microbiology Reviews, Vol. 33, Issue 2 https://doi.org/10.1111/j.1574-6976.2008.00134.x	journal	March 2009
Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms Orr, James C.; Fabry, Victoria J.; Aumont, Olivier Nature, Vol. 437, Issue 7059 https://doi.org/10.1038/nature04095	journal	September 2005
Iron Constraints on Planktonic Primary Production in Oligotrophic Lakes Vrede, Tobias; Tranvik, Lars J. Ecosystems, Vol. 9, Issue 7 https://doi.org/10.1007/s10021-006-0167-1	journal	November 2006
Light-Induced Energy Dissipation in Iron-Starved Cyanobacteria: Roles of OCP and IsiA Proteins Wilson, Adjélé; Boulay, Clémence; Wilde, Annegret The Plant Cell, Vol. 19, Issue 2 https://doi.org/10.1105/tpc.106.045351	journal	February 2007
The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving Photosystem II complex Papageorgiou, George C.; Murata, Norio Photosynthesis Research, Vol. 44, Issue 3 https://doi.org/10.1007/BF00048597	journal	June 1995

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Title: Coping with iron limitation: A metabolomic study of Synechocystis sp. PCC 6803

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