Effect of iron speciation on growth and heat resistance of Symbiodiniaceae
DOI:
https://doi.org/10.1590/2675-2824070.21103jmdrKeywords:
Chelate, Heat shock, Lipophilicity, Photosynthetic dinoflagellates, Bioinorganic chemistryAbstract
Iron is a limiting nutrient for Symbiodiniaceae (colloquially known as zooxanthellae), with low solubility in seawater. The use of stable, soluble, and chemically defined iron complexes is proposed as a strategy to control the supply of this metal to target organisms. In this work, we investigated the effect of iron(II) and derivatives of iron(III) (desferrioxamine, deferiprone, deferasirox, and HBED) over the growth and metal loading of five Symbiodiniaceae species. Iron supplementation did not affect growth or metal load in species with high iron stocks. In contrast, for species with low iron stocks, hydrophobic Fe(DFX)2 was very efficient in inducing growth and iron loading. Also, the desferrioxamine derivative of iron Fe(DFO) appeared as an interesting, ecologically friendly source of the nutrient. The effect of iron supplementation on the growth of Breviolum minutum submitted to heat shock was also studied. Iron supplementation prior to the heat shock episode increased the heat tolerance of B. minutum. Such findings provide new insights for the strategy of iron supplementation to improve the fitness of Symbiodiniaceae, both in vitro and in the environment.
References
AMIN, S. A., GREEN, D. H., GARDES, A., ROMANO, A., TRIMBLE, L. & CARRANO, C. J. 2012. Siderophore-mediated iron uptake in two clades of Marinobacter spp. associated with phytoplankton: the role of light. Biometals, 25(1), 181-192.
ANDEREGG, G., LEPLATTE, F. & SCHWARZENBACH, G. 1963. Hydroxamatkomplexe .3. Eisen(III)-austausch zwischen sideraminen und komplexonen - diskussion der bildungskonstanten der hydroxamatkomplexe. Helvetica Chimica Acta, 46, 1409-&.
ANDEREGG, G., SCHWARZENBACH, G. & LEPLATTE.F. 1963. Hydroxamatkomplexe .2. Die anwendung der ph-methode. Helvetica Chimica Acta, 46, 1400-&.
AUMONT, O. & BOPP, L. 2006. Globalizing results from ocean in situ iron fertilization studies. Global Biogeochemical Cycles, 20(2).
BALZANO, S., SARDO, A., BLASIO, M., CHAHINE, T. B., DELL’ANNO, F., SANSONE, C. & BRUNET, C. 2020. Microalgal metallothioneins and phytochelatins and their potential use in bioremediation. Frontiers in Microbiology, 11, 517.
BANNOCHIE, C. J. & MARTELL, A. E. 1989. Affinities of racemic and meso forms of n,n’-ethylenebis 2-(ortho-hydroxyphenyl)glycine for divalent and trivalent metal-ions. Journal of the American Chemical Society, 111, 4735-4742.
BICKEL, H., HALL, G. E., KELLERSCHIERLEIN, W., PRELOG, V., VISCHER, E. & WETTSTEIN, A. 1960. Stoffwechselprodukte von actinomyceten .27. Uber die konstitution von ferrioxamin-B. Helvetica Chimica Acta, 43, 2129-2138.
BISCERE, T., FERRIER-PAGES, C., GILBERT, A., PICHLER, T. & HOULBREQUE, F. 2018. Evidence for mitigation of coral bleaching by manganese. Scientific Reports, 8.
BLABY-HAAS, C. E. & MERCHANT, S. S. 2012. The ins and outs of algal metal transport. Biochimica Et Biophysica Acta-Molecular Cell Research, 1823(9), 1531-1552.
BOZHKOV, A., PADALKO, V., DLUBOVSKAYA, V. & MENZIANOVA, N. 2010. Resistance to heavy metal toxicity in organisms under chronic exposure. Indian Journal of Experimental Biology, 48(7), 679-696.
CHOUDHARY, N., SCHEIBER, H., ZHANG, J. L., PATRICK, B. O., JARAQUEMADA-PELAEZ, M. D. & ORVIG, C. 2021. H(4)HBEDpa: octadentate chelate after A. E. Martell. Inorganic Chemistry, 60(17), 12855-12869.
CSASZAR, N. B. M., SENECA, F. O. & VAN OPPEN, M. J. H. 2009. Variation in antioxidant gene expression in the scleractinian coral Acropora millepora under laboratory thermal stress. Marine Ecology Progress Series, 392, 93-102.
DAVY, S. K., ALLEMAND, D. & WEIS, V. M. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews, 76(2), 229-261.
DESCHASEAUX, E., JONES, G. & SWAN, H. 2016. Dimethylated sulfur compounds in coral-reef ecosystems. Environmental Chemistry, 13(2), 239-251.
EPLATTENIER, F. L., MURASE, I. & MARTELL, A. 1967. New multidentate ligands. VI. Chelating Tendencies of N,n2-Di(2-hydroxybenzyl)ethylenediamine-N,n2-diacetic Acid. Journal of the American Chemical Society, 89, 837-843.
EVERS, A., HANCOCK, R. D., MARTELL, A. E. & MOTEKAITIS, R. J. 1989. Metal-ion recognition in ligands with negatively charged oxygen donor groups - complexation of FE(III), GA(III), IN(III), AL(III), and other highly charged metal-ions. Inorganic Chemistry, 28(11), 2189-2195.
FERRIER-PAGES, C., SCHOELZKE, V., JAUBERT, J., MUSCATINE, L. & HOEGH-GULDBERG, O. 2001. Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrichment. Journal of Experimental Marine Biology and Ecology, 259(2), 249-261.
GORDON, R. M., JOHNSON, K. S. & COALE, K. H. 1998. The behaviour of iron and other trace elements during the IronEx-I and PlumEx experiments in the Equatorial Pacific. Deep-Sea Research Part Ii-Topical Studies in Oceanography, 45(6), 995-1041.
GUILLARD, R. R. L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: SMITH, W. L. & CHANLEY, M. H. (eds.). Culture of marine invertebrate animals. Boston: Springer, pp. 29-60.
HATTON, A. D. & WILSON, S. T. 2007. Particulate dimethylsulphoxide and dimethylsulphoniopropionate in phytoplankton cultures and Scottish coastal waters. Aquatic Sciences, 69(3), 330-340.
HEINZ, U., HEGETSCHWEILER, K., ACKLIN, P., FALLER, B., LATTMANN, R. & SCHNEBLI, H. P. 1999. 4-3,5-bis(2-hydroxyphenyl)-1,2,4-triazol-1-yl benzoic acid: a novel efficient and selective iron(III) complexing agent. Angewandte Chemie-International Edition, 38, 2568-2570.
HOPKINSON, B. M. & MOREL, F. M. M. 2009. The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals, 22(4), 659-669.
IGLESIAS-PRIETO, R., MATTA, J. L., ROBINS, W. A. & TRENCH, R. K. 1992. Photosynthetic response to elevated-temperature in the symbiotic dinoflagellate symbiodinium-microadriaticum in culture. Proceedings of the National Academy of Sciences of the United States of America, 89(21), 10302-10305.
KAKHLON, O., BREUER, W., MUNNICH, A. & CABANTCHIK, Z. I. 2010. Iron redistribution as a therapeutic strategy for treating diseases of localized iron accumulation. Canadian Journal of Physiology and Pharmacology, 88(3), 187-196.
KARPISHIN, T. B., GEBHARD, M. S., SOLOMON, E. I. & RAYMOND, K. N. 1991. Spectroscopic studies of the electronic-structure of iron(iii) tris(catecholates). Journal of the American Chemical Society, 113(8), 2977-2984.
KRACHLER, R., KRACHLER, R., VALDA, A. & KEPPLER, B. K. 2019. Natural iron fertilization of the coastal ocean by “blackwater rivers”. Science of the Total Environment, 656, 952-958.
LAJEUNESSE, T. C., PARKINSON, J. E., GABRIELSON, P. W., JEONG, H. J., REIMER, J. D., VOOLSTRA, C. R. & SANTOS, S. R. 2018. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28(16), 2570-2580.
LIN, C., CHONG, G., WANG, L. H., KUO, F. W. & TSAI, S. 2019. Use of luminometry and flow cytometry for evaluating the effects of cryoprotectants in the gorgonian coral endosymbiont Symbiodinium. Phycological Research, 67, 320-326.
LUND, J. W. G., KIPLING, C. & LE CREN, E. D. 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia, 11, 143-170.
MARTIN, J. H. & FITZWATER, S. E. 1988. Iron-deficiency limits phytoplankton growth in the northeast pacific subarctic. Nature, 331, 341-343.
MARTIN, J. H., GORDON, R. M. & FITZWATER, S. E. 1990. Iron in antarctic waters. Nature, 345, 156-158.
MATTOS, A. L. C., CONSTANTINO, V. R. L., COUTO, R. A. A., PINTO, D. M. L., KANEKO, T. M. & ESPOSITO, B. P. 2013. Desferrioxamine-cadmium as a ‘Trojan horse’ for the delivery of Cd to bacteria and fungi. Journal of Trace Elements in Medicine and Biology, 27(2), 103-108.
MCGINTY, E. S., PIECZONKA, J. & MYDLARZ, L. D. 2012. Variations in reactive oxygen release and antioxidant activity in multiple symbiodinium types in response to elevated temperature. Microbial Ecology, 64(4), 1000-1007.
MERCHANT, S. S., ALLEN, M. D., KROPAT, J., MOSELEY, J. L., LONG, J. C., TOTTEY, S. & TERAUCHI, A. M. 2006. Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochimica et Biophysica Acta-Molecular Cell Research, 1763, 578-594.
MIES, M., GUTH, A. Z., CASTRO, C. B., PIRES, D. O., CALDERON, E. N., POMPEU, M. & SUMIDA, P. Y. G. 2018. Bleaching in reef invertebrate larvae associated with Symbiodinium strains within clades A-F. Marine Biology, 165(1).
MONZYK, B. & CRUMBLISS, A. L. 1982. Kinetics and mechanism of the stepwise dissociation of iron(iii) from ferrioxamine-b in aqueous acid. Journal of the American Chemical Society, 104(18), 4921-4929.
MUSCATINE, L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. In: DUBINSKY, Z. (ed.). Ecosystems of the world. Amsterdam: Elsevier, pp. 75-87.
MUSCATINE, L. & PORTER, J. W. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience, 27(7), 454-460.
NAITO, K., IMAI, I. & NAKAHARA, H. 2008. Complexation of iron by microbial siderophores and effects of iron chelates on the growth of marine microalgae causing red tides. Phycological Research, 56(1), 58-67.
NODWELL, L. M. & PRICE, N. M. 2001. Direct use of inorganic colloidal iron by marine mixotrophic phytoplankton. Limnology and Oceanography, 46(4), 765-777.
NOVARTIS. 2020. Highlights of prescribing information - Exjade(R) [leaflet] New Jersey: Novartis Pharmaceutics Corporation.
NURCHI, V. M., CRISPONI, G., ARCA, M., CRESPO-ALONSO, M., LACHOWICZ, J. I., MANSOORI, D., TOSO, L., PICHIRI, G., SANTOS, M. A., MARQUES, S. M., NICLOS-GUTIERREZ, J., GONZALEZ-PEREZ, J. M., DOMINGUEZ-MARTIN, A., CHOQUESILLO-LAZARTE, D., SZEWCZUK, Z., ZORODDU, M. A. & PEANA, M. 2014. A new bis-3-hydroxy-4-pyrone as a potential therapeutic iron chelating agent. Effect of connecting and side chains on the complex structures and metal ion selectivity. Journal of Inorganic Biochemistry, 141, 132-143.
OECD (Organisation for Economic Co-operation and Development). 1995. Test No. 107: partition coefficient (n-octanol/water): shake flask method Paris: OECD Publishing.
PERALES-VELA, H. V., PENA-CASTRO, J. M. & CANIZARES-VILLANUEVA, R. O. 2006. Heavy metal detoxification in eukaryotic microalgae. Chemosphere, 64(1), 1-10.
PICCIANI, N., SEIBLITZ, I., PAIVA, P. C., CASTRO, C. B. E. & ZILBERBERG, C. 2016. Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the Southwestern Atlantic Ocean. Marine Biology, 163(1), 1-11.
REICH, H. G., RODRIGUEZ, I. B., LAJEUNESSE, T. C. & HO, T. Y. 2020. Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae. Coral Reefs, 39(4), 915-927.
REICH, H. G., TU, W. C., RODRIGUEZ, I. B., CHOU, Y. L., KEISTER, E. F., KEMP, D. W., LAJEUNESSE, T. C. & HO, T. Y. 2021. Iron availability modulates the response of endosymbiotic dinoflagellates to heat stress. Journal of Phycology, 57, 3-13.
RODRIGUEZ, I. B., LIN, S., HO, J. & HO, T. Y. 2016. Effects of trace metal concentrations on the growth of the coral endosymbiont Symbiodinium kawagutii. Frontiers in Microbiology, 7, 82
ROFF, G. & MUMBY, P. J. 2012. Global disparity in the resilience of coral reefs. Trends in Ecology & Evolution, 27(7), 404-413.
ROSIC, N. N., PERNICE, M., DOVE, S., DUNN, S. & HOEGH-GULDBERG, O. 2011. Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress & Chaperones, 16(1), 69-80.
SAUVAGE, J., WIKFORS, G. H., SABBE, K., NEVEJAN, N., GODERIS, S., CLAEYS, P., LI, X. X. & JOYCE, A. 2021. Biodegradable, metal-chelating compounds as alternatives to EDTA for cultivation of marine microalgae. Journal of Applied Phycology, 33, 3519-3537, DOI: https://doi.org/10.1007/s10811-021-02583-0
» https://doi.org/10.1007/s10811-021-02583-0
SHAKED, Y., KUSTKA, A. B. & MOREL, F. M. M. 2005. A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnology and Oceanography, 50(3), 872-882.
SHICK, J. M., IGLIC, K., WELLS, M. L., TRICK, C. G., DOYLE, J. & DUNLAP, W. C. 2011. Responses to iron limitation in two colonies of Stylophora pistillata exposed to high temperature: Implications for coral bleaching. Limnology and Oceanography, 56(3), 813-828.
SONG, P. C., WU, T. M., HONG, M. C. & CHEN, M. C. 2015. Elevated temperature inhibits recruitment of transferrin-positive vesicles and induces iron-deficiency genes expression in Aiptasia pulchella host-harbored Symbiodinium. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 188, 1-7.
STEINHAUSER, S., HEINZ, U., BARTHOLOMA, M., WEYHERMULLER, T., NICK, H. & HEGETSCHWEILER, K. 2004. Complex formation of ICL670 and related ligands with Fe-III and Fe-II. European Journal of Inorganic Chemistry, 2004(21), 4177-4192, DOI: https://doi.org/10.1002/ejic.200400363
» https://doi.org/10.1002/ejic.200400363
TAYLOR, K. G. & KONHAUSER, K. O. 2011. Iron in earth surface systems: a major player in chemical and biological processes. Elements, 7(2), 83-87.
TRICK, C. G., BILL, B. D., COCHLAN, W. P., WELLS, M. L., TRAINER, V. L. & PICKELL, L. D. 2010. Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proceedings of the National Academy of Sciences of the United States of America, 107(13), 5887-5892.
USSHER, S. J., ACHTERBERG, E. P. & WORSFOLD, P. J. 2004. Marine biogeochemistry of iron. Environmental Chemistry, 1(2), 67-80.
