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Biosorption of thorium on the external shell surface of bivalve mollusks: The role of shell surface microtopography

Biosorption of thorium on the external shell surface of bivalve mollusks: The role of shell surface microtopography
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  This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institutionand sharing with colleagues.Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third partywebsites are prohibited.In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further informationregarding Elsevier’s archiving and manuscript policies areencouraged to visit:  Author's personal copy Biosorption of thorium on the external shell surface of bivalve mollusks: The roleof shell surface microtopography Michael Zuykov a, ⇑ , Emilien Pelletier a , Richard Saint-Louis b , Antonio Checa c , Serge Demers a a Institut des sciences de la mer de Rimouski (ISMER), Université du Québec à Rimouski, Rimouski, 310, allée des Ursulines, QC, Canada G5L 3A1 b Department of Biology, Chemistry and Geography, Université du Québec à Rimouski, Rimouski, 310, allée des Ursulines, QC, Canada G5L 3A1 c Department of Stratigraphy and Paleontology, University of Granada, Avenida Fuentenueva s/n, 18071 Granada, Spain a r t i c l e i n f o  Article history: Received 30 July 2011Received in revised form 9 November 2011Accepted 11 November 2011Available online 7 December 2011 Keywords: ThoriumBiosorptionBivalveShell surfaceMicrotopographyLA-ICP-MS a b s t r a c t External shell surface (ESS) of bivalve mollusks is known to adsorb various metals dissolved in ambientwater in high concentration. It is hypothesized here that the surface microtopography of the thin organiccoating layer, periostracum, or calcareous shell (if periostracum was destroyed) plays a major role in theadsorption of actinides on ESS. Thorium (natural alpha-emitter) was used in short-term biosorptionexperiment with shell fragments of five bivalve mollusks. After a 72h exposure to Th (  6kBqL   1 ), tho-rium concentration was measured on ESS using laser ablation inductively coupled plasma mass spec-trometry; the distribution and density of alpha tracks were subsequently visualized by  a -trackautoradiography.AtrendinreducedThconcentrationsontheESSwasobserveddependinguponthespe-cies tested: (group 1  4000 l gg  1 )  Chlamys islandica  (M.),  Mercenaria mercenaria  (L.),  Dreissena polymor- pha  (P.)>(group 2  1200 l gg  1 )  Crassostrea virginica  (G.)  (group 3  150 l gg  1 )  Mytilus edulis  L. Themicrotopography of ESS was characterized by scanning electron microscopy revealing the high porosityof the calcareous surface of   C. islandica  and  M. mercenaria , lamellate surface of periostracum in  D. poly-morpha , uneven but a weakly porous surface of periostracum of   C. virginica , and a nearly smooth surfaceof the periostracum of   M. edulis . This work has demonstrated, for the first time, the presence of a strongcorrelation between concentration of adsorbed Th and ESS microtopography, and the role of the perios-tracum in this process is discussed.   2011 Elsevier Ltd. All rights reserved. 1. Introduction Previous investigations (Bertine and Goldberg, 1972; Hamiltonand Clifton, 1980; Koide et al., 1982; Miramand et al., 1982;McDonald et al., 1993a,b; Zuykov et al., 2009, 2011; Metian et al.,2011) of metal and actinide concentrations in the bivalve molluskshells obtained after laboratory experiments or determined fromenvironmental samples have demonstrated the followingfeatures:(1) The content of metals recorded in shells can often be higherthan in soft tissues, and metals in shells have longer biolog-ical half-lives.(2) Thedataavailableinnumerouspapersarebasedonthecon-tent of metals on the external shell surface (ESS), whereastheir concentrations on the internal shell surface are toolow and considered negligible.(3) ConcentrationofmetalsonESSdiffersbetweentaxaandalsodepends on the nature of the metal itself.To the best of our knowledge, none of these studies have ad-dressed any relationship between measured metal concentrationsand the microtopography of ESS, for both model Mytilidae speciesand other bivalve taxa. The interdependency between chemicalcomposition, roughness, porosity of ESS and the ability of ESS toadsorb metals should be logically examined as the specific natureof any artificial or biological surface is expected to be related toits sorption properties. Using thorium as a model actinide, thepresent paper assesses the role of ESS microtopography in theadsorption of Th in the marine bivalves  Chlamys islandica ,  Crassos-trea virginica ,  Mercenaria mercenaria ,  Mytilus edulis , and in thefreshwater bivalve  Dreissena polymorpha , after a short term bio-sorption experiment using shell fragments. 2. Materials and methods Fifty-three (53) shell fragments (5  10mm) with visually nonabradedESSwerecutfromthesameareas(Fig.1A–E)ofadultshellsof   C. islandica  (shell length, sl=150mm),  C. virginica  (sl=80mm), D. polymorpha  (sl=25mm),  M. mercenaria  (sl=40mm), and  M.edulis  (sl=60mm). Bivalves were grown in our laboratory (IS-MER-UQAR), sampled from clean environment or purchased from 0045-6535/$ - see front matter    2011 Elsevier Ltd. All rights reserved.doi:10.1016/j.chemosphere.2011.11.023 ⇑ Corresponding author. Tel.: +1 418 732 8357; fax: +1 418 724 1842. E-mail address: (M. Zuykov).Chemosphere 86 (2012) 680–683 Contents lists available at SciVerse ScienceDirect Chemosphere journal homepage:  Author's personal copy seafood store. Before experiments the shell fragments obtainedfrom freshly sampled animals were washed in distilled water inan ultrasonic bath for 30min. Preliminary geochemical analysisshowed the absence of thorium in any detectable amount in theESS of all samples.ExperimentswerecarriedoutineightTefloncontainerscontain-ing20mLofthoriumsolutionpreparedfromasolutionofdissolvedThin1%nitricacidinnanopurewater(ThoriumEnviroConcentrate)purchased from Ultra Scientific ( as a thoriumstandardforICP-MScalibration.TheradioactivityofThinwaterali-quots was measured bygamma-spectrometryand was foundto be  6kBqL   1 in six replicate containers with shells of all speciesmixed together (up to 10 fragments in each container); and   3and 4kBqL   1 was measured in two additional containers whereonly shells of   C. islandica  and  M. edulis  were placed (2 samples ineach container). As actinides tend to form strong complexes withdifferent ligands present in seawater (Choppin, 2006) that could interferewithThavailabilityandtheadsorptionprocess,deionizedwater was used as an experimental medium and EDTA (ethylenediaminetetraaceticacid)wasaddedtothesolutionatanequimolarconcentrationwiththoriumto preventanyprecipitationof Th. ThepH of the solution was adjusted to 8.2 (to equal that of the marineenvironment) using 1.0M NaOH. The solutions with shell frag-ments were shaken every 8h for 5min of the exposure period(72h). Subsequently, shell fragments were carefully washed threetimeswithdistilledwateranddriedatambientroomtemperature.A quadrupole ICP-MS (Agilent 7500c, USA) interfaced with a la-serablationsystem(NewWaveResearchUP213,USA)wasusedtoquantify Th adsorbed on the ESS in eighteen (18) shell fragments.LA-ICP-MS line scans can provide equivalent or better informationabout the distributionof elements in heterogeneous solid samples,e.g. the ESS, than discrete spot analysis (Sanborn and Telmer,2003). On the ESS of each shell fragment after focusing, three linepaths, with a length 750 l m each, were ablated (laser wavelength,213nm; energy output of 50%; rep rate, 5Hz; beam diameter,40 l m; scanning speed, 20 l ms  1 ) with helium as the carrier gasmixed with argon as the make-up gas via a T-connector beforeentering the ICP torch. The signal (CPS, count per second) of Thwas measured at  m /  z   =232. The ESS concentration of thorium ex-pressedas l gg  1 wascalculatedbasedonthesignalofThobtainedunder the same LA-ICP-MS conditions from the microanalyticalcarbonatestandardMACS-3(UnitedStatesGeologicalSurveyrefer-ence materials program, USA). The matrix of the standard is a cal-cium carbonate (like calcareous part of mollusks shell) containingThat a recommended valueof 55.4±1.1 l gg  1 (Chenet al., 2011).Therelative standarddeviationof the Thsignal fromMACS-3anal-ysis was 17% ( n  =18).Forpreparationof  a -trackautoradiograms,shellsweremountedincross-sectionwithinroundsupportswhichwerethenfilledwithacrylic resin (Struers Inc.). After curing of the resin, the plastic tab-lets were polished and covered by individual pieces of   a -sensitivecellulosenitratefilm(commerciallyavailableasLR-115typeII, Ko-dak; After an exposure periodof 30d, the films were etched in 6M NaOH for 230min at 50  C,carefully washed with distilled water and dried at 35  C for 1h.The  a -tracks were examined and photographed with an opticalmicroscope Olympus under x100 magnification. For preparationof microphotographs of ESS, the surface of the samples was coatedwith gold–palladium and studied with scanning electron micros-copy (JEOL JSM-6460 LV) using an acceleration voltage of 20kV. 3. Results  3.1. Microtopography of ESS  Ultrathin periostracum (<1 l m) fragments were preserved onESSin C.islandica and M.mercenaria .Theshellsof  C.islandica areen-tirelycalcitic,exceptforthearagoniticmyostracum;theoutermostlayerismadeoffinecalciticfibres,whichmakearelativelysmoothESS penetrated by micrometric irregular cavities (Fig. 1A). In con-trast,in M. mercenaria  theESSis formedbythetopsof fibrouspris-matic crystals of aragonite, the boundaries of which appear in lowrelief;natural etchingprovidesthesurfaceappreciablyhighporos-ity (Fig. 1B).  D. polymorpha  has a thin(5–7 l m), but well preserved   A 1 A 2 A  2 B 1 BB C D E 1 C 1 D  2 E 1 E   Fig. 1.  Microtopography of the external surface of shell fragments of   Chlamys islandica  (A),  Mercenaria mercenaria  (B),  Dreissena polymorpha  (C),  Crassostrea virginica  (D), Mytilus edulis  (E) selectedfor the present study (studiedzones in quadrates) withvarious magnification. SEMimages are labeled with numbers (1, 2).  P   – periostracum. Scalebars (a–e) 10mm. M. Zuykov et al./Chemosphere 86 (2012) 680–683  681  Author's personal copy periostracum, which emits frequent lamellae, thus forming a com-plicated surface (Fig. 1C). The ESS of   C. virginica  consists of a thinperiostracum with elevated surface roughness that, however, hasa low porosity (Fig. 1D). Finally, a thick periostracum (35–40 l m)withapracticallysmoothsurfaceis preservedin M. edulis  (Fig. 1E).  3.2. Concentration of thorium on ESS  The concentration of thoriumon ESS measured with LA-ICP-MSdiffers significantly (One-way ANOVA,  p  <0.001) among the spe-cies tested. Three groups can be distinguished on the basis of theTh concentration found on the ESS (Fig. 2) .  The minimal variationsin Th concentrations between line scans are only in  M. edulis  thatshowstherelativelyhomogenousdistributionofThinthematricesexamined. As the laser ablation technique was perforating the ESSto the depth of about 30–40 l m (Fig. 3), the measured concentra-tions include all possible Th adsorbed onto the ESS due to its poorpenetration inside the shell (Fig. 4).  3.3. Shell autoradiography The density of   a -tracks associated with ESS, as shown on auto-radiograms, strongly differs between  C. islandica  and  M. edulis (Fig. 4). No important differences in a -track densities are observedbetween shells of other species, as well as between shells of  C. islandica  and  M. edulis  exposed to three different concentrations.The central part in all shells always remains free from  a -tracksconfirming the absence of Th within the calcareous shell. 4. Discussion Partitioning of some metals(e.g. actinides and gamma-emittingradionuclides) between the ESS and the internal shell surface (ISS)wasbrieflystudied.Methodologically,itwasbasedonindependentmeasurements of metal contents in mechanically removed perios-tracum and in scraped calcareous shell. For example, McDonaldet al. (1993a) reported that 96% of   239+240 Pu, 95% of   238 Pu, 98% of  95 Nb, 97%of  137 Cswerefoundintheperiostracumofthebluemus-sel  M. edulis  collected from the environment. At the same time, inthe present study the shell fragments of   M. edulis  with a thickwell-preserved periostracum exhibited the lowest concentrationof Th on the ESS, whereas the highest Th concentration was ad-  C.  i s l a n d i c a M. m e r c e n a r i a D. p o l y m o r p h a C. v i r g i n i c a M. e d u l i s 2000400060000       )      g        /     g      µ        (      n    o       i      t     a     r      t     n    e     c     n    o       C  I gr II gr III gr  Fig. 2.  Grouping of studied mollusks on the basis of Th concentrations detected ontheexternalshell surfaceineachlinescan. Errorbarsrepresentstandarddeviations(for  D. polymorpha n  =6, for others  n  =12). Fig. 3.  TraceofthelinescanafterLA-ICP-MSontheexternal shell surfaceof  Mytilusedulis .SEMimages.Periostracumandunderlyingminerallayersweredestroyed(A),line scan in shell cross section (B). ESSISS contour of shell rib ESSISS AB Fig. 4.  Alpha-track distribution in shells (cross section) of   Chlamys islandica  (A) and Mytilus edulis  (B) after 72h exposure with Th. ESS – external shell surface, ISS –internal shell surface. Scale bars 100 l m.682  M. Zuykov et al./Chemosphere 86 (2012) 680–683  Author's personal copy sorbed on the ESS of   C. islandica  and  M. mercenaria  with an ultra-thin and poorly preserved periostracum. On the other hand, theESS in  D. polymorpha  with a thin periostracum is characterizedby a high Th concentration because of very peculiar lamellate sur-face of its periostracum. Consequently, the presence of an intactperiostracum (and its thickness) does not guarantee an enhancedability of the ESS to adsorb Th among the species tested, whereas,in the first instance, it has a strong correlation with microtopogra-phy of ESS. In theory, another explanation could be related to theeffective antifouling properties of the periostracum which may in-clude a chemical mode of action that is as yet poorly studied (Tay-lor and Kennedy, 1969; Wahl et al., 1998; Scardino et al., 2003). Inthis context it is interesting to note that in  Corbicula fluminea  (M.)the biochemistry of periostracum can be modified after exposuretosomeorganiccontaminants(Meenakshietal., 1969;Hutchinsonet al., 1993a,b). In any case, if this holds true for all actinides (e.g.almost identical distribution of U, Pu, and Am in shells of   M. edulis has been confirmed (Hamilton, 1980; Hamilton and Clifton, 1980)this result is of critical importance for the detection of transuranicradionuclides, because classical biological tool used in many bio-monitoring studies,  M. edulis , has shown a significantly lower acti-nide concentration in comparison with the other tested species.  Acknowledgments Theauthorsaregrateful toC. Gagnon(EnvironmentCanada)fordonation of   D. polymorpha  specimens and S. Fowler for helpful dis-cussion.Wegratefullyacknowledgetheassistancewithbiosorptionexperiments by I. Desbiens (ISMER). This work was supported byNSERCDiscoveryGrants(E.P.andS.D).ThisisacontributionofQue-bec-Ocean network. References Bertine, K.K., Goldberg, E.D., 1972. Trace elements in clams, mussels, and shrimp.Limnol. Oceanogr. 17, 877–884.Chen, L., Liu, Y., Hu, Z., Gao, S., Zong, K., Chen, H., 2011. Accurate determinations of fifty-four major and trace elements in carbonate by LA-ICP-MS usingnormalizationstrategy of bulk components as 100%. Chem. Geol. 284, 283–295.Choppin, G.R., 2006. Actinide speciation in aquatic systems. Mar. Chem. 99, 83–92.Hamilton,E.I.,1980.Concentrationanddistributionofuraniumin Mytilus edulis  andassociated materials. Mar. Ecol. -Prog. 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