A synergetic biomineralization strategy for immobilizing strontium during calcification of the coccolithophore Emiliania huxleyi
The coccolithophore species Emiliania huxleyi has one of the most global distributions in the modern oceans. They are characteristically covered with calcite scales called coccoliths. In this study, stable strontium immobilization during the calcification process was investigated to indirectly assess a proposed bioremediation approach for removing Sr2+ contamination from marine environments. Results indicate that E. huxleyi has high Sr2+ tolerance and removal efficiency in response to Sr2+ stress ranging from 5.6 to 105.6 ppm. Sr2+ immobilization during E. huxleyi calcification indicates a concentration-dependent synergistic mechanism. At lower concentrations of Sr2+ (25.6 ppm), Sr2+ is incorporated into coccoliths through competitive supply between Sr2+ and Ca2+. In addition, calcite productivity decreases with increased Sr2+ removal efficiency due to crystallographic transformation of coccoliths from hydrated calcite into aragonite at 55.6 ppm Sr2+. Further formation of strontianite at 105.6 ppm Sr2+ is due to precipitation of Sr2+ on the edge of the rims and radial arrays of the coccoliths. Our study implies that coccolithophores are capable of significant removal of Sr2+ from the marine environment.
KeywordsCalcification Coccolithophores Biological purification Strontium immobilization Biomineralization
The present work was partly supported by the National Natural Science Foundation of China (41472310, 41502316), National Basic Research Program of China (973 Program: 2014CB846003), and The Longshan Academic Talent Research Support Program of the Southwest University of Science and Technology (17LZX419, 17LZXT05). We thanks Mr. Biaobiao Ma for helping revise the manuscript.
- Benzerara K, Skouri-Panet F, Li J, Ferard C, Gugger M, Laurent T, Couradeau E, Ragon M, Cosmidis J, Menguy N, Margaret-Oliver I, Tavera R, Lopez-Garcia P, Moreira D (2014) Intracellular Ca-carbonate biomineralization is widespread in cyanobacteria. Proc Natl Acad Sci U S A 111(30):10933–10938. https://doi.org/10.1073/pnas.1403510111 CrossRefGoogle Scholar
- Langer G, Gussone N, Nehrke G, Riebesell U, Eisenhauer A, Kuhnert H, Rost B, Trimborn S, Thoms S (2006) Coccolith strontium to calcium ratios in Emiliania huxleyi: the dependence on seawater strontium and calcium concentrations. Limnol Oceanogr 51(1):310–320. https://doi.org/10.4319/lo.2006.51.1.0310 CrossRefGoogle Scholar
- Liu M, Dong F, Zhang W, Nie X, Sun S, Wei H, Luo L, Xiang S, Zhang G (2016) Programmed gradient descent biosorption of strontium ions by Saccaromyces cerevisiae and ashing analysis: a decrement solution for nuclide and heavy metal disposal. J Hazard Mater 314:295–303. https://doi.org/10.1016/j.jhazmat.2016.04.049 CrossRefGoogle Scholar
- Povinec PP, Hirose K, Aoyama M (2012) Radiostrontium in the western North Pacific: characteristics, behavior, and the Fukushima impact. Environ Sci Technol 46:10356Google Scholar
- Price NM, Harrison GI, Hering JG, Hudson RJ, Nirel PMV, Palenik B, Morel FMM (1988) Preparation and chemistry of the artificial algal culture medium Aquil. Biol Oceanogr 6:443–461Google Scholar
- Rodriguez-Navarro C, Jroundi F, Schiro M, Ruiz-Agudo E, González-Muñoz MT (2012) Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: implications for stone conservation. Appl Environ Microbiol 78(11):4017–4029. https://doi.org/10.1128/AEM.07044-11 CrossRefGoogle Scholar
- Shozugawa K, Riebe B, Walther C, Brandl A, Steinhauser G (2016) Fukushima-derived radionuclides in sediments of the Japanese Pacific Ocean coast and various Japanese water samples (seawater, tap water, and coolant water of Fukushima Daiichi reactor unit 5). J Radioanal Nucl Chem 307(3):1787–1793. https://doi.org/10.1007/s10967-015-4386-9 CrossRefGoogle Scholar
- Stevenson EI, Hermoso M, REM R, Tyler JJ, Minoletti F, Parkinson IJ, Mokadem F, Burton KW (2014) Controls on stable strontium isotope fractionation in coccolithophores with implications for the marine Sr cycle. Geochim Cosmochim Acta 128:225–235. https://doi.org/10.1016/j.gca.2013.11.043 CrossRefGoogle Scholar
- Sun S, Yao Y, Zou X, Fan S, Zhou Q, Dai Q, Dong F, Liu M, Nie X, Tan D, Li S (2014) Nano-scale spatial assessment of calcium distribution in Coccolithophores using synchrotron-based nano-CT and STXM-NEXAFS. Int J Mol Sci 15(12):23604–23615. https://doi.org/10.3390/ijms151223604 CrossRefGoogle Scholar
- Tazaki K, Shimojima Y, Takehara T, Nakano M (2015) Formation of microbial mats and salt in radioactive paddy soils in Fukushima, Japan. Fortschr Mineral 5:0529Google Scholar
- Zou X, Sun S, Lin S, Shen K, Dong F, Tan D, Nie X, Liu M, Wei J (2017) Calcification response of Pleurochrysis carterae to iron concentrations in batch incubations: implication for the marine biogeochemical cycle. Front Earth Sci 11(4):682–688. https://doi.org/10.1007/s11707-016-0629-5 CrossRefGoogle Scholar