Abstract
Biominerals are widespread in Nature and they precipitate to respond to different physiological purposes. A broad knowledge of their chemical and structural properties offers a unique opportunity to improve our capability to reconstruct actual and paleoenvironment. In this work, we show two case studies, bivalves and foraminifera grown in polluted sites that were characterized by applying different and complementary synchrotron radiation-based investigation techniques, mainly focused on the investigation of Zn incorporation in the biomineralized shells. Using scanning transmission X-ray microscopy (STXM) and X-ray micro-fluorescence (µ-XRF), we found the colocalization of elements across the shells, while we obtained information on chemical speciation of Zn by applying X-ray absorption spectroscopy (XAS). Noticeably, instead of metal dispersion in the Ca-carbonate shells, we found traces of several independent phases, in particular for Zn, dispersed generally as microscopic minerals. This work provides fundamental insight into the structural properties, coordinative and chemical environment of some marine biominerals. This new knowledge is fundamental to understand the biogeochemical processes and to develop effective environmental proxies.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
E. Beniash, Biominerals—hierarchical nanocomposites: the example of bone. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 3, 47–69 (2011). https://doi.org/10.1002/wnan.105
J. Yu, H. Elderfield, Benthic foraminiferal B/Ca ratios reflect deep water carbonate saturation state. Earth Planet. Sci. Lett. 258, 73–86 (2007). https://doi.org/10.1016/j.epsl.2007.03.025
D.W. Lea, G.T. Shen, E.A. Boyle, Coralline barium records temporal variability in equatorial Pacific upwelling. Nature 340, 373–376 (1989). https://doi.org/10.1038/340373a0
S.P. Bryan, T.M. Marchitto, Testing the utility of paleonutrient proxies Cd/Ca and Zn/Ca in benthic foraminifera from thermocline waters. Geochem. Geophys. Geosyst. 11, Q01005 (2010). https://doi.org/10.1029/2009GC002780
A.L. Soldati, D.E. Jacob, P. Glatzel, J.C. Swarbrick, J. Geck, Element substitution by living organisms: the case of manganese in mollusc shell aragonite. Sci. Rep. 6, 22514 (2016). https://doi.org/10.1038/srep22514
L. Chauvaud, A. Lorrain, R.B. Dunbar, Y.-M. Paulet, G. Thouzeau, F. Jean, J.-M. Guarini, D. Mucciarone, Shell of the Great Scallop Pecten maximus as a high-frequency archive of paleoenvironmental changes. Geochem. Geophys. Geosyst. 6, 1–15 (2005). https://doi.org/10.1029/2004GC000890
M.H. Klünder, D. Hippler, R. Witbaard, D. Frei, Laser ablation analysis of bivalve shells—archives of environmental information. Geol. Surv. Denmark Greenl. Bull. 15, 89–92 (2008)
A.J. Gooday, Benthic foraminifera (protista) as tools in deep-water palaeoceanography: environmental influences on faunal characteristics. Adv. Mar. Biol. 46, 1–90 (2003). https://doi.org/10.1016/S0065-2881(03)46002-1
E. Armynot du Châtelet, J.-P. Debenay, R. Soulard, Foraminiferal proxies for pollution monitoring in moderately polluted harbors. Environ. Pollut. 127, 27–40 (2004). https://doi.org/10.1016/S0269-7491(03)00256-2
G. Nehrke, H. Poigner, D. Wilhelms-Dick, T. Brey, D. Abele, Coexistence of three calcium carbonate polymorphs in the shell of the Antarctic clam Laternula elliptica. Geochem. Geophys. Geosyst. 13, 1–8 (2012). https://doi.org/10.1029/2011GC003996
S. Weiner, H.A. Lowenstam, L. Hood, Characterization of 80-million-year-old mollusk shell proteins. Proc. Natl. Acad. Sci. U. S. A. 73, 2541–2545 (1976). https://doi.org/10.1073/pnas.73.8.2541
A. Checa, A new model for periostracum and shell formation in Unionidae (Bivalvia, Mollusca). Tissue Cell. 32, 405–416 (2000). https://doi.org/10.1054/tice.2000.0129
Z. Yao, M. Xia, H. Li, T. Chen, Y. Ye, H. Zheng, Bivalve shell: not an abundant useless waste but a functional and versatile biomaterial. Crit. Rev. Environ. Sci. Technol. 44, 2502–2530 (2014). https://doi.org/10.1080/10643389.2013.829763
M. Suzuki, S. Sakuda, H. Nagasawa, Identification of chitin in the prismatic layer of the shell and a chitin synthase gene from the Japanese pearl oyster. Pinctada Fucata. Biosci. Biotechnol. Biochem. 71, 1735–1744 (2007). https://doi.org/10.1271/bbb.70140
Y. Kong, G. Jing, Z. Yan, C. Li, N. Gong, F. Zhu, D. Li, Y. Zhang, G. Zheng, H. Wang, L. Xie, R. Zhang, Cloning and characterization of Prisilkin-39, a novel matrix protein serving a dual role in the prismatic layer formation from the oyster Pinctada fucata. J. Biol. Chem. 284, 10841–10854 (2009). https://doi.org/10.1074/jbc.M808357200
R.A. Lutz, Bivalve Molluscs: biology, ecology and culture by Elizabeth Gosling. Q. Rev. Biol. 79, 317 (2004). https://doi.org/10.1086/425799
L.J. De Nooijer, H.J. Spero, J. Erez, J. Bijma, G.J. Reichart, Biomineralization in Perforate Foraminifera. Earth-Sci. Rev. 135, 48–58 (2014). https://doi.org/10.1016/j.earscirev.2014.03.013
S. Weiner, P.M. Dove, An overview of biomineralization processes and the problem of the vital effect. Rev. Mineral. Geochem. 54, 1–29 (2003). https://doi.org/10.2113/0540001
B.R. Schöne, D.P. Gillikin, Unraveling environmental histories from skeletal diaries—advances in sclerochronology. Palaeogeogr. Palaeoclimatol. Palaeoecol. 373, 1–5 (2013). https://doi.org/10.1016/j.palaeo.2012.11.026
J. Erez, The source of ions for biomineralization in Foraminifera and their implications for paleoceanographic proxies. Rev. Mineral. Geochem. 54, 115–149 (2003). https://doi.org/10.2113/0540115
G.M. Henderson, New oceanic proxies for paleoclimate. Earth Planet. Sci. Lett. 203, 1–13 (2002). https://doi.org/10.1016/S0012-821X(02)00809-9
M. Risk, M. Burchell, K. de Roo, R. Nairn, M. Tubrett, G. Försterra, Trace elements in bivalve shells from the Río Cruces, Chile. Aquat. Biol. 10, 85–97 (2010). https://doi.org/10.3354/ab00268
J. Yu, H. Elderfield, B. Hönisch, B/Ca in planktonic foraminifera as a proxy for surface seawater pH. Paleoceanography 22, PA2202 (2007). https://doi.org/10.1029/2006PA001347
J.E. Pietrzak, J.M. Bates, R.M. Scott, Constituents of unionoid extrapalial fluid. II. pH and metal ion composition. Hydrobiologia 50, 89–93 (1976)
M. Zuykov, E. Pelletier, C. Belzile, S. Demers, Alteration of shell nacre micromorphology in blue mussel Mytilus edulis after exposure to free-ionic silver and silver nanoparticles. Chemosphere 84, 701–706 (2011). https://doi.org/10.1016/j.chemosphere.2011.03.021
V. Yanko, A.J. Arnold, W.C. Parker, Effects of Marine Pollution on Benthic Foraminifera—Modern Foraminifera (Springer, Netherlands, Dordrecht, 2003)
R.J.P. Williams, J.J.R.F. da Silva, The Natural Selection of the Chemical Elements (Bath Press Ltd., Great Britian, 1996)
X.-M. Liu, L.C. Kah, A.H. Knoll, H. Cui, A.J. Kaufman, A. Shahar, R.M. Hazen, Tracing Earth’s O2 evolution using Zn/Fe ratios in marine carbonates. Geochemical Perspect. Lett. 2, 24–34 (2016). https://doi.org/10.7185/geochemlet.1603
P.B. Tchounwou, C.G. Yedjou, A.K. Patlolla, D.J. Sutton, Heavy metal toxicity and the environment. Exp. Suppl. 101, 133–164 (2012). https://doi.org/10.1007/978-3-7643-8340-4_6
R. Singh, N. Gautam, A. Mishra, R. Gupta, Heavy metals and living systems: An overview. Indian J. Pharmacol. 43, 246–253 (2011). https://doi.org/10.4103/0253-7613.81505
D. Medas, I. Carlomagno, C. Meneghini, G. Aquilanti, T. Araki, D.E. Bedolla, C. Buosi, M.A. Casu, A. Gianoncelli, A.C. Kuncser, V.A. Maraloiu, G.D. Giudici, Zinc incorporation in marine bivalve shells grown in mine-polluted seabed sediments : a case study in the Malfidano mining area ( SW Sardinia, Italy ). Environ. Sci. Pollut. Res. (2018). https://doi.org/10.1007/s11356-018-3504-y
G. De Giudici, C. Meneghini, D. Medas, C. Buosi, P. Zuddas, A. Iadecola, O. Mathon, A. Cherchi, A.C. Kuncser, Coordination environment of Zn in foraminifera Elphidium aculeatum and Quinqueloculina seminula shells from a polluted site. Chem. Geol. 477, 100–111 (2018). https://doi.org/10.1016/j.chemgeo.2017.12.009
T. Bechstädt, M. Boni, Sedimentological, stratigraphical and ore deposits field guide of the autochthonous Cambro-Ordovician of southwestern Sardinia: Servizio Geologico d’Italia Memorie Descritive Carta Geologica d’Italia, v. 48, 434 p. (1994)
A. Marcello, S. Pretti, P. Valera, M. Agus, M. Boni, M. Fiori, Metallogeny in Sardinia (Italy): from the Cambrian to the Tertiary, in 32nd International Geological Congress, APAT 4, ed. by L. Guerrieri, L. Rischia, L. Serva, pp. 14–36, Firenze (2004)
M. Boni, H.A. Gilg, G. Aversa, G. Balassone, The “Calamine” of Southwest Sardinia: geology, mineralogy, and stable isotope geochemistry of supergene Zn mineralization. Econ. Geol. 98, 731–748 (2003). https://doi.org/10.2113/gsecongeo.98.4.731
P. Stara, R. Rizzo, G.A. Tanca, Iglesiente-Arburese: Miniere e Minerali, Centrooffset, Siena (1996)
R. Bartole, S. De Muro, Acoustic facies and seabed features of the mixed carbonate-siliciclastic deposits of the last eustatic cycle in the La Maddalena Archipelago (North Sardinia, Italy). Ital. J. Geosci. 131, 102–122 (2012). https://doi.org/10.3301/IJG.2011.28
M. Schintu, B. Marras, A. Maccioni, D. Puddu, P. Meloni, A. Contu, Monitoring of trace metals in coastal sediments from sites around Sardinia. Western Mediterranean. Mar. Pollut. Bull. 58, 1577–1583 (2009). https://doi.org/10.1016/j.marpolbul.2009.07.015
V. Moschino, M. Schintu, A. Marrucci, B. Marras, N. Nesto, L. Da Ros, An ecotoxicological approach to evaluate the effects of tourism impacts in the Marine Protected Area of La Maddalena (Sardinia, Italy). Mar. Pollut. Bull. 122, 306–315 (2017). https://doi.org/10.1016/j.marpolbul.2017.06.062
G. Salvi, C. Buosi, D. Arbulla, A. Cherchi, G. De Giudici, A. Ibba, S. De Muro, Ostracoda and foraminifera response to a contaminated environment: the case of the Ex-military arsenal of the la Maddalena Harbour (Sardinia, Italy). Micropaleontology 61, 115–133 (2015)
W.R. Walton, Techniques for recognition of living foraminifera. Contrib. Cushman. Found. Foraminifer. Res. 3, 56–60 (1952)
A.R. Loeblich Jr., H. Tappan, Foraminiferal Genera and Their Classification (Van Reinhold Company, New York, 1987)
F. Cimerman, M.R. Langer, Mediterranean Foraminifera. Ljubljana, Slovenska Akademija Znanosti in Umetnosti. Academia Scientiarum et ArtiumSlovencia Cl. 4 Historia Naturalis (1991)
L. Hottinger, E. Halicz, Z. Reiss, Recent Foraminiferida from the Gulf of Aqaba, Red Sea. Lubljana Academia Scientiarum et ArtiumSlovenica, Classis IV, Historia Naturalis (1993)
F. Sgarrella, M. Moncharmont Zei, Benthic foraminifera of the Gulf of Naples (Italy): systematics and autoecology. Boll. Soc. Paleontol. Ital. 32, 145–264 (1993)
D.E. Conners, S.M. Westerfield, A. Feyko, M.C. Black, Lead Accumulation in soft tissues and shells of asiatic clams (Corbicula fluminea), in The 1999 Georgia Water Resources Conference, ed. by K. J. Hatcher, pp. 597–600 (1999)
A. Gianoncelli, G.R. Morrison, B. Kaulich, D. Bacescu, J. Kovac, Scanning transmission x-ray microscopy with a configurable detector. Appl. Phys. Lett. 89, 251117–251119 (2006). https://doi.org/10.1063/1.2422908
G.R. Morrison, A. Gianoncelli, B. Kaulich, D. Bacescu, J. Kovac, A fast readout CCD system for configured-detector imaging in STXM, in Proceedings of the 8th International Conference X-ray Microscopy. IPAP Conference Series, pp. 277–379 (2006)
A. Gianoncelli, B. Kaulich, R. Alberti, T. Klatka, A. Longoni, A. de Marco, A. Marcello, M. Kiskinova, Simultaneous soft X-ray transmission and emission microscopy. Nucl. Instrum. Methods Phys. Res. Sect. A Accel. Spectrometers, Detect. Assoc. Equip. 608, 195–198 (2009). https://doi.org/10.1016/j.nima.2009.06.035
A. Gianoncelli, G. Kourousias, A. Stolfa, B. Kaulich, Recent developments at the TwinMic beamline at ELETTRA: an 8 SDD detector setup for low energy X-ray Fluorescence. J. Phys. Conf. Ser. 425, 182001 (2013). https://doi.org/10.1088/1742-6596/425/18/182001
A. Gianoncelli, G. Kourousias, L. Merolle, M. Altissimo, A. Bianco, Current status of the TwinMic beamline at Elettra: a soft X-ray transmission and emission microscopy station. J. Synchrotron Radiat. 23, 1526–1537 (2016). https://doi.org/10.1107/S1600577516014405
A. Gianoncelli, G. Kourousias, M. Altissimo, D.E. Bedolla, L. Merolle, A. Stolfa, H.-J. Shin, Combining multiple imaging techniques at the TwinMic X-ray microscopy beamline. AIP Conf. Proc. 1764, 30002 (2016). https://doi.org/10.1063/1.4961136
B. Kaulich, D. Bacescu, J. Susini, C. David, E. Di Fabrizio, G.R. Morrison, P. Charalambous, J. Thieme, T. Wilhein, J. Kovac, D. Cocco, M. Salome, O. Dhez, T. Weitkamp, S. Cabrini, D. Cojoc, A. Gianoncelli, U. Vogt, M. Podnar, M. Zangrando, M. Zacchigna, M. Kiskinova, Proceeding 8th International Conference X‐ray Microscopy IPAP Conference Series. Presented at the (2006)
Numpy: https://docs.scipy.org/doc/numpy-1.14.0/reference/generated/numpy.corrcoef.html. Copyright 2008–2009, The Scipy community. Last updated on 11 May 2014
scipy: https://docs.scipy.org/doc/scipy-0.14.0/reference/generated/scipy.stats.spearmanr.html. Copyright 2008–2009, The Scipy community. Last updated on 11 May 2014
A. Di Cicco, G. Aquilanti, M. Minicucci, E. Principi, N. Novello, A. Cognigni, L. Olivi, Novel XAFS capabilities at ELETTRA synchrotron light source. J. Phys. Conf. Ser. 190, 12043 (2009). https://doi.org/10.1088/1742-6596/190/1/012043
M. Benfatto, C. Meneghini, A close look into the low energy region of the XAS spectra: the XANES region, in Synchrotron Radiation, Basic, Methods and Applications, ed. by S. Mobilio, F. Boscherini, C. Meneghini (Springer-Verlag, Berlin, 2014), pp. 213–240
R. Torchio, C. Meneghini, S. Mobilio, G. Capellini, A. Garcia Prieto, J. Alonso, M.L. Fdez-Gubieda, V. Turco Liveri, A. Longo, A.M. Ruggirello, T. Neisius, Microstructure and magnetic properties of colloidal cobalt nano-clusters. J. Magn. Magn. Mater. 322, 3565–3571 (2010). https://doi.org/10.1016/j.jmmm.2010.07.008
C. Meneghini, F. Bardelli, S. Mobilio, ESTRA-FitEXA: a software package for EXAFS data analysis. Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. Atoms. 285, 153–157 (2012). https://doi.org/10.1016/j.nimb.2012.05.027
O. Mathon, A. Beteva, J. Borrel, D. Bugnazet, S. Gatla, R. Hino, I. Kantor, T. Mairs, M. Munoz, S. Pasternak, F. Perrin, S. Pascarelli, The time-resolved and extreme conditions XAS (TEXAS) facility at the European Synchrotron Radiation Facility: the general-purpose EXAFS bending-magnet beamline BM23. J. Synchrotron Radiat. 22, 1548–1554 (2015). https://doi.org/10.1107/S1600577515017786
C.K. Carney, S.R. Harry, S.L. Sewell, Detoxification biominerals, in Biomineralization I. Topics in Current Chemistry, ed. by K. Naka (Springer, Berlin, Heidelberg, 2007), pp. 155–185
V. Le Cadre, J.-P. Debenay, Morphological and cytological responses of Ammonia (foraminifera) to copper contamination: implication for the use of foraminifera as bioindicators of pollution. Environ. Pollut. 143, 304–317 (2006). https://doi.org/10.1016/j.envpol.2005.11.033
Acknowledgements
We acknowledge CESA (grant number: E58C16000080003) from RAS, and RAS/FBS (grant number: F72F16003080002) grants, the POR FESR Sardegna 2014-2020 (project cluster Top-Down: TESTARE), and the CeSAR (Centro Servizi d’Ateneo per la Ricerca) of the University of Cagliari, Italy, for SEM analysis. The ESRF EV-94 and ES-540 proposals provided access to the BM23 micro-focus experiment. The authors acknowledge the CERIC-ERIC Consortium (grant numbers: 20152020, 20162061, 20167045, 20177041, and 20182100) for the access to experimental facilities and financial support and the Romanian Ministry of Education (through the Core Program, Project PN16-480102). XAFS (Elettra) 20160254 beamtime, Diamond SP16496 beamtime, and grant are acknowledged. The research leading to this result has been supported by the project CALIPSOplus under the Grant Agreement 730872 from the EU Framework Program for Research and Innovation HORIZON 2020. The Grant of Excellence Departments, MIUR (ARTICOLO 1, COMMI 314–337 LEGGE 232/2016), is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this paper
Cite this paper
De Giudici, G. et al. (2021). Zn Distribution and Chemical Speciation in Marine Biominerals: An Example on Bivalve and Foraminifera Shells from Polluted Sites. In: Di Cicco, A., Giuli, G., Trapananti, A. (eds) Synchrotron Radiation Science and Applications. Springer Proceedings in Physics, vol 220. Springer, Cham. https://doi.org/10.1007/978-3-030-72005-6_10
Download citation
DOI: https://doi.org/10.1007/978-3-030-72005-6_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-72004-9
Online ISBN: 978-3-030-72005-6
eBook Packages: Physics and AstronomyPhysics and Astronomy (R0)