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

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Abstract

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. In addition, 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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Acknowledgements

The authors thank Laia Mateu-Castell, Laura Steger, Zarraz Lee, Jessica Corman, Krist Rouypirom, Zureyma Martinez, Matthew Kellom, Wei Deng, and Jennifer Learned for their laboratory support. Thanks to Ravi Vannela for providing Synechocystis sp. PCC 6803 and Wim Vermaas for the helpful discussion of the data. ARU appreciates the financial support of the research fellowship (JAE) from the CSIC. This research was supported by the Spanish Government Project CGL2013-48074-P and the Catalan Government Project SGR 2014-274, the European Research Council (Synergy Grant SyG-2013-610028, IMBALANCE-P), and the NASA Astrobiology Institute at Arizona State University (Follow the Elements; NAI5-0018). A portion of the research was performed using EMSL, a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research at the Pacific Northwest National Laboratory. MO and OU were supported by the Ministry of Education, the National Sustainability Program I (NPU I), grants LO1415 and LM2015061, and by CzeCOS ProCES project num. CZ.02.1.01/0.0/0.0/16_013/0001609. ATPP and JJE were supported by the ASU NASA Astrobiology Institute.

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Author notes

  1. Amisha T. Poret-Peterson

    Present address: USDA-ARS, Crops Pathology and Genetics Research Unit, University of California, Davis, CA, 95616, USA

  2. Albert Rivas-Ubach and Amisha T. Poret-Peterson have contributed equally to the manuscript.

Authors and Affiliations

  1. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, 3335 Innovation Boulevard, Richland, WA, 99354, USA

    Albert Rivas-Ubach

  2. CREAF, Cerdanyola del Vallès, 08913, Catalonia, Spain

    Albert Rivas-Ubach, Josep Peñuelas & Jordi Sardans

  3. School of Earth and Space Exploration, Arizona State University, Tempe, AZ, 85287, USA

    Amisha T. Poret-Peterson

  4. CSIC, Global Ecology Unit CREAF-CEAB-CSIC-UAB, Cerdanyola del Vallès, 08913, Catalonia, Spain

    Josep Peñuelas & Jordi Sardans

  5. Service of Nuclear Magnetic Resonance, Faculty of Sciences and Biosciences, Universitat Autònoma de Barcelona, Bellaterra, 08193, Barcelona, Catalonia, Spain

    Míriam Pérez-Trujillo

  6. King’s College London, Institute of Pharmaceutical Science, London, SE1 9NH, England, UK

    Cristina Legido-Quigley

  7. Global Change Research Institute, Czech Academy of Sciences, Bĕlidla 986/4a, 603 00, Brno, Czech Republic

    Michal Oravec & Otmar Urban

  8. School of Life Sciences, Arizona State University, Tempe, AZ, 85287-4501, USA

    James J. Elser

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Rivas-Ubach, A., Poret-Peterson, A.T., Peñuelas, J. et al. Coping with iron limitation: a metabolomic study of Synechocystis sp. PCC 6803. Acta Physiol Plant 40, 28 (2018). https://doi.org/10.1007/s11738-018-2603-1

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