Coping with iron limitation: a metabolomic study of Synechocystis sp. PCC 6803
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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.
KeywordsMetabolomics Metallomics Iron limitation Cyanobacteria Ecological stoichiometry
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.
- da Silva JJRF, Williams RJP (2001) The biological chemistry of the elements: the inorganic chemistry of life. Oxford University Press, New York, pp 1–583. ISBN: 0198508484Google Scholar
- Dejean S, Gonzalez I, Le Cao K (2013) mixOmics: Omics Data Integration Project. R package version 5.0-1. http://CRAN.R-project.org/package=mixOmics
- Fox J, Weisberg S (2011) An R companion to applied regression. R package, 2nd edn. Sage, Thousand Oaks CA. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
- Kellom M, Poret-Peterson AT, Rivas-Ubach A et al (2018) Transcriptomics of iron limitation without growth media chelation in the cyanobacterium Synechocystis sp. PCC 6803 (Submitted) Google Scholar
- Krieg N, Parte A, Ludwig W et al (2010) Bergey’s manual of systematic bacteriology, vol 4. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. Springer, New YorkGoogle Scholar
- Lengeler J, Drews G, Schlegel H (1999) Biology of the prokaryotes. Wiley-Blackwell, Hoboken, pp 1–984Google Scholar
- Oksanen J, Guillaume-Blanchet F, Kindt R et al (2013) vegan: community ecology package. R package version 2.0-9. http://CRAN.R-project.org/package=vegan
- R Core Team (2013) R: a language and environment for statistical computing. R packageGoogle Scholar
- Sterner R, Elser J (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, pp 1–439. ISBN: 0691074909Google Scholar
- Vitousek PM, Aber JD, Howarth RW et al (1997) Human alteration of the global nitrogen cycle: sources and cosequences. Ecol Appl 7:737–750Google Scholar