Variability in the production of organic ligands, by Synechococcus PCC 7002, under different iron scenarios
Several Fe-uptake mechanisms suggest the importance of the presence of certain organic ligands in phytoplankton exudates. Here, it has been studied how Synechococcus (strain PCC 7002) acclimates to Fe-bioavailability, comparing the growth and organic exudation under two different Fe regimes. These cyanobacteria were incubated in UV-treated seawater supplemented only with major nutrients and two different iron scenarios (Low-Fe and High-Fe), without chelating agents, in order to analyze the organic ligands production. The levels of dissolved organic carbon (DOC) and two natural ligands (hydroxamic and phenolic moieties) were monitored. The responses in the organic extracellular release rates (ER), normalized per cell, were statistically analyzed considering Fe scenarios and different development stages. Growth of Synechococcus was significantly slower under Low-Fe treatment, suggesting that these cultures were iron limited compared to those flourished with higher levels of iron in the medium. Although the concentration of DOC increased to 127.13 ± 8.38 and 150.51 ± 8.59 μmol C L−1 under Low-Fe and High-Fe conditions, respectively, no-significant variations were found in the DOCER, among growth phases and iron bioavailability scenarios. Under High-Fe conditions, the production of hydroxamic ligands was inhibited, while the extracellular release rate of phenolic compounds decreased, regarding to Low-Fe conditions. Growth phases of Synechococcus also modified the extracellular release rates both of hydroxamic and phenolic moieties. The present study, therefore, demonstrates that iron availability and growth stages might be key parameters in regulating the release performance of extracellular Fe-specific organic ligands by cyanobacteria.
KeywordsSynechococcus Iron Extracellular release Organic ligands Cyanobacteria Fe-bioavailability
This study received supported from EACFe Project (CTM2014-52342-P) of the Ministerio de Economía y Competitividad of Spain. G. S. R. participation was supported by the Grant BES-2011-051448 of the Ministerio de Economía y Competitividad. The authors thank Dr. Javier Aristegui and IOCAG for the measurements of dissolved organic carbon. We gratefully acknowledge the comments and suggestions of the anonymous reviewers.
- Arnow LE (1937) Colorimetric determination of the components of 3,4-dihydroxyphenylalaninetyrosine mixtures. J Biol Chem 118:531–537Google Scholar
- Behrenfeld MJ, Milligan AJ (2011) Photophysiological expressions of iron stress in phytoplankton. Ann Rev Marine Sci 5:120717164858000. https://doi.org/10.1146/annurev-marine-121211-172356 Google Scholar
- Cadier M, Gorgues T, Sourisseau M et al (2017) Assessing spatial and temporal variability of phytoplankton communities’ composition in the Iroise Sea ecosystem (Brittany, France): a 3D modeling approach. Part 1: biophysical control over plankton functional types succession and distribution. J Mar Syst 165:47–68. https://doi.org/10.1016/j.jmarsys.2016.09.009 CrossRefGoogle Scholar
- Lelong A, Bucciarelli E, Hégaret H, Soudant P (2013) Iron and copper limitations differently affect growth rates and photosynthetic and physiological parameters of the marine diatom Pseudo-nitzschia delicatissima. Limnol Oceanogr 58:613–623. https://doi.org/10.4319/lo.2013.58.2.0613 CrossRefGoogle Scholar
- Payne SM (1994) Bacterial pathogenesis part A: identification and regulation of virulence factors. In: Clark V (ed) Bavoil P. Academic Press, CambridgeGoogle Scholar
- Simpson FB, Neilands JB (1976) Siderochomes in cyanophyceae: isolation and characterization of schizokinen from Anabaena sp 1. J Phycol 12:44–48. https://doi.org/10.1111/j.1529-8817.1976.tb02824.x Google Scholar
- Strzepek RF, Maldonado MT, Hunter KA et al (2011) Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: uptake of organically complexed iron and reduced cellular iron requirements. Limnol Oceanogr 56:1983–2002. https://doi.org/10.4319/lo.2011.56.6.1983 CrossRefGoogle Scholar
- Verweij W (2017) Computer program for calcultaling the Chemical Equilibria in AQuatic Systems (CHEAQS-Next). Version 2017.3Google Scholar
- Vraspir JM, Butler A (2009) Chemistry of marine ligands and siderophores. Ann Rev Marine Sci 1:43–63. https://doi.org/10.1146/annurev.marine.010908.163712 CrossRefGoogle Scholar
- Williams PJB, Quay PD, Westberry TK, Behrenfeld MJ (2013) The Oligotrophic Ocean is autotrophic. Ann Rev Marine Sci 5:535–549. https://doi.org/10.1146/annurev-marine-121211-172335 CrossRefGoogle Scholar