Abstract
Aquatic organisms that inhabit coastal areas are often exposed to several contaminants. It is known that the bioaccumulation of contaminants can be amplified according to the species feeding habits and contaminant properties. As a consequence, species can experience different effects to contaminant exposure even if they inhabit the same area. The present study aimed to investigate the activities of carbonic anhydrase (CA), Ca2+-ATPase, and Mg2+-ATPase in different tissues (soft tissue, mantle, and gill) of three mollusk species (Lottia subrugosa, Stramonita brasiliensis, and Crassostrea brasiliana) with different feeding habits (herbivore, carnivore, and filter-feeder, respectively) which were sampled within a known contamination gradient at Santos Estuarine System (Southeastern Brazil). From the three enzymes tested, only CA was affected by the presence of contaminants within the contamination gradient evaluated. In general, the CA activity from the three species were lower in contaminated sites when compared to the reference site. The contrasting CA activity response observed in S. brasiliensis compared to L. subrugosa and C. brasiliana could be related to the tissue-specificity of this enzyme activity and species feeding habits (filter-feeders can accumulate more contaminants than herbivores and even carnivores). Results indicated that C. brasiliana mantle is the most suitable tissue for the use of CA analysis as a biomarker.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abessa DMS, Zaroni LP, de Sousa ECPM et al. (2005) Physiological and cellular responses in two populations of the mussel Perna perna collected at different sites from the coast of São Paulo, Brazil. Brazilian Arch Biol Technol 48:217–225. https://doi.org/10.1590/s1516-89132005000200008
Abreu FEL, Lima da Silva JN, Castro ÍB, Fillmann G (2020) Are antifouling residues a matter of concern in the largest South American port? J Hazard Mater 398:122937. https://doi.org/10.1016/j.jhazmat.2020.122937
Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. In: Methods in Enzymology. Academic Press, pp 115–118
Azevedo-Linhares M, Freire CA (2015) Evaluation of impacted Brazilian estuaries using the native oyster Crassostrea rhizophorae: Branchial carbonic anhydrase as a biomarker. Ecotoxicol Environ Saf 122:483–489. https://doi.org/10.1016/j.ecoenv.2015.09.027
Begliomini FN, Maciel DC, de Almeida SM et al. (2017) Shell alterations in limpets as putative biomarkers for multi-impacted coastal areas. Environ Pollut 226:494–503. https://doi.org/10.1016/j.envpol.2017.04.045
Blaise C, Gagné F, Burgeot T (2017) Three simple biomarkers useful in conducting water quality assessments with bivalve mollusks. Environ Sci Pollut Res 24:27662–27669. https://doi.org/10.1007/s11356-016-6908-6
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Burlando B, Bonomo M, Caprì F et al. (2004) Different effects of Hg2+ and Cu2+ on mussel (Mytilus galloprovincialis) plasma membrane Ca2+-ATPase: Hg2+ induction of protein expression. Comp Biochem Physiol Part C Toxicol Pharmacol 139:201–207. https://doi.org/10.1016/J.CCA.2004.11.001
Buruaem LM, Castro ÍB, Hortellani MA et al. (2013) Integrated quality assessment of sediments from harbour areas in Santos-São Vicente Estuarine System, Southern Brazil. Estuar Coast Shelf Sci 130:179–189. https://doi.org/10.1016/J.ECSS.2013.06.006
Cabrini TMB, Barboza CAM, Skinner VB et al. (2018) Investigating heavy metal bioaccumulation by macrofauna species from different feeding guilds from sandy beaches in Rio de Janeiro, Brazil. Ecotoxicol Environ Saf 162:655–662. https://doi.org/10.1016/j.ecoenv.2018.06.077
Caricato R, Giordano ME, Schettino T et al. (2019) Carbonic anhydrase integrated into a multimarker approach for the detection of the stress status induced by pollution exposure in Mytilus galloprovincialis: A field case study. Sci Total Environ 690:140–150. https://doi.org/10.1016/j.scitotenv.2019.06.446
Caricato R, Giordano ME, Schettino T, Lionetto MG (2018) Functional involvement of carbonic anhydrase in the lysosomal response to cadmium exposure in Mytilus galloprovincialis digestive gland. Front Physiol 9:319. https://doi.org/10.3389/fphys.2018.00319
Caricato R, Lionetto MG, Dondero F et al. (2010) Carbonic anhydrase activity in Mytilus galloprovincialis digestive gland: Sensitivity to heavy metal exposure. Comp Biochem Physiol - C Toxicol Pharmacol 152:241–247. https://doi.org/10.1016/j.cbpc.2010.04.011
Castro ÍB (2019) Improper environmental sampling design bias assessments of coastal contamination. Trends Environ Anal Chem 24:e00068. https://doi.org/10.1016/j.teac.2019.e00068
Catharino MGM, Vasconcellos MBA, Kirschbaum AA et al. (2015) Passive biomonitoring study and effect biomarker in oysters Crassostrea brasiliana (Lamark, 1819: Mollusca, Bivalvia) in Santos and Cananéia Estuaries in São Paulo State, Brazil. J Radioanal Nucl Chem 303:2297–2302. https://doi.org/10.1007/s10967-014-3720-y
Chapman MG (1997) Relationships between shell shape, water reserves, survival and growth of highshore littorinids under experimental conditions in New South Wales, Australia. J Molluscan Stud 63:511–529. https://doi.org/10.1093/MOLLUS/63.4.511
Diederich CM, Bashevkin SM, Chaparro OR, Pechenik JA (2015) Desiccation tolerance and lifting behavior in Crepidula fornicata (Gastropoda). Mar Ecol Prog Ser 528:235–243. https://doi.org/10.3354/meps11284
dos Santos MB, Monteiro Neto IE, de Souza Melo SRC, Amado EM (2017) Hemolymph and gill carbonic anhydrase are more sensitive to aquatic contamination than mantle carbonic anhydrase in the mangrove oyster Crassostrea rhizophorae. Comp Biochem Physiol Part - C Toxicol Pharmacol 201:19–25. https://doi.org/10.1016/j.cbpc.2017.08.008
Erulkar SD (1981) The versatile role of calcium in biological systems. Interdiscip Sci Rev 6:322–332. https://doi.org/10.1179/isr.1981.6.4.322
Ferraz MA, Choueri RB, Castro ÍB et al. (2020) Influence of sediment organic carbon on toxicity depends on organism’s trophic ecology. Environ Pollut 261:114134. https://doi.org/10.1016/j.envpol.2020.114134
Galloway TS, Brow R, Browne MA et al. (2004) A multibiomarker approach to environmental assessment. Environ Sci Technol 38:1723–1731. https://doi.org/10.1021/es030570
Gimiliani GT, Fontes RFC, Abessa DMS (2016) Modeling the dispersion of endocrine disruptors in the Santos Estuarine System (Sao Paulo State, Brazil). Brazilian J Oceanogr 64:1–8. https://doi.org/10.1590/S1679-87592016072806401
Gouveia N, Oliveira CRM, Martins CP et al. (2019) Can shell alterations in limpets be used as alternative biomarkers of coastal contamination? Chemosphere 224:9–19. https://doi.org/10.1016/j.chemosphere.2019.02.122
Harayashiki CAY, Márquez F, Cariou E, Castro ÍB (2020) Mollusk shell alterations resulting from coastal contamination and other environmental factors. Environ Pollut 265:114881. https://doi.org/10.1016/j.envpol.2020.114881
Harayashiki CAY, Sadauskas-Henrique H, de Souza-Bastos LR et al. (2021) Shell form and enzymatic alterations in Lottia subrugosa (Gastropoda, Lotiidae) transplanted to a contaminated site. Mar Pollut Bull 164:112075. https://doi.org/10.1016/j.marpolbul.2021.112075
Hickey CW, Roper DS, Holland PT, Trower TM (1995) Accumulation of organic contaminants in two sediment-dwelling shellfish with contrasting feeding modes: Deposit- (<i>Macomona liliana<i>) and filter-feeding (<i>Austrovenus stutchburyi<i>). Arch Environ Contam Toxicol 29:221–231. https://doi.org/10.1007/BF00212973
Jorge MB, Loro VL, Bianchini A et al. (2013) Mortality, bioaccumulation and physiological responses in juvenile freshwater mussels (Lampsilis siliquoidea) chronically exposed to copper. Aquat Toxicol 126:137–147. https://doi.org/10.1016/j.aquatox.2012.10.014
Kaag NHBM, Foekema EM, Scholten MCT, van Straalen NM (1997) Comparison of contaminant accumulation in three species of marine invertebrates with different feeding habits. Environ Toxicol Chem 16:837–842. https://doi.org/10.1002/etc.5620160501
Kim BSM, Angeli JLF, Ferreira PA, de L et al. (2017) Use of a chemometric tool to establish the regional background and assess trace metal enrichment at Baixada Santista – southeastern Brazil. Chemosphere 166:372–379. https://doi.org/10.1016/j.chemosphere.2016.09.132
Liao Z, Jiang YY-TYT, Sun Q et al. (2019) Microstructure and in-depth proteomic analysis of Perna viridis shell. PLoS One 14:e0219699. https://doi.org/10.1371/journal.pone.0219699
Lionetto M, Caricato R, Giordano M et al. (2012) Carbonic anhydrase as pollution biomarker: An ancient enzyme with a new use. Int J Environ Res Public Health 9:3965–3977. https://doi.org/10.3390/ijerph9113965
Lionetto M, Caricato R, Giordano M, Schettino T (2016) The complex relationship between metals and carbonic anhydrase: New insights and perspectives. Int J Mol Sci 17:127. https://doi.org/10.3390/ijms17010127
Lionetto MG, Caricato R, Erroi E, et al. (2006) Potential application of carbonic anhydrase activity in bioassay and biomarker studies. Chem Ecol 22: https://doi.org/10.1080/02757540600670661
Mann K, Edsinger-Gonzales E, Mann M (2012) In-depth proteomic analysis of a mollusc shell: acid-soluble and acid-insoluble matrix of the limpet Lottia gigantea. Proteome Sci 10:28. https://doi.org/10.1186/1477-5956-10-28
Mann K, Edsinger E (2014) The Lottia gigantea shell matrix proteome: Re-analysis including MaxQuant iBAQ quantitation and phosphoproteome analysis. Proteome Sci 12: https://doi.org/10.1186/1477-5956-12-28
Marin F, Le Roy N, Marie B (2012) The formation and mineralization of mollusk shell. Front Biosci (Schol Ed) 4:1099–1125
Nikinmaa M (2014) An Introduction to Aquatic Toxicology. Elsevier Inc.
Nozadze E, Arutinova N, Tsakadze L et al. (2015) Molecular mechanism of Mg-ATPase activity. J Membr Biol 248:295–300. https://doi.org/10.1007/s00232-014-9769-2
Oh DJ, Hur SP, Bouchekioua S et al. (2018) Tide-related changes in mRNA abundance of aromatases and estrogen receptors in the ovary and brain of the threespot wrasse Halichoeres trimaculatus. Ocean Sci J 53:239–249. https://doi.org/10.1007/s12601-018-0016-0
Oliveira CRM, Mantovani de Castro L, Alves da Cruz Nazareth M et al. (2020) Shell structure and composition alterations in the limpet Lottia subrugosa along a contamination gradient in the Santos Estuary, Brazil. Ecol Indic 115:106417. https://doi.org/10.1016/j.ecolind.2020.106417
Pattnaik S, Chainy GBN, Jena JK (2007) Characterization of Ca2+-ATPase activity in gill microsomes of freshwater mussel, Lamellidens marginalis (Lamarck) and heavy metal modulations. Aquaculture 270:443–450. https://doi.org/10.1016/J.AQUACULTURE.2007.05.012
Pivovarova NB, Lagerspetz KYH, Skulskii IA (1992) Effect of cadmium on ciliary and ATPase activity in the gills of freshwater mussel Anodonta cygnea. Comp Biochem Physiol Part C Comp Pharmacol 103:27–30. https://doi.org/10.1016/0742-8413(92)90223-T
Pusceddu FH, Sugauara LE, de Marchi MR et al. (2019) Estrogen levels in surface sediments from a multi-impacted Brazilian estuarine system. Mar Pollut Bull 142:576–580. https://doi.org/10.1016/j.marpolbul.2019.03.052
Rittschof D, McClellan-Green P (2005) Molluscs as multidisciplinary models in environment toxicology. Mar Pollut Bull 50:369–373. https://doi.org/10.1016/J.MARPOLBUL.2005.02.008
Santini O, Chahbane N, Vasseur P, Frank H (2011) Effects of low-level copper exposure on Ca2+-ATPase and carbonic anhydrase in the freshwater bivalve Anodonta anatina. Toxicol Environ Chem 93:1826–1837. https://doi.org/10.1080/02772240903217598
Sokolova IM, Pörtner HO (2001) Temperature effects on key metabolic enzymes in Littorina saxatilis and L. Obtusata from different latitudes and shore levels. Mar Biol 139:113–126. https://doi.org/10.1007/s002270100557
Supuran C (2008) Carbonic anhydrases - An overview. Curr Pharm Des 14:603–614. https://doi.org/10.2174/138161208783877884
Supuran CT (2016) Structure and function of carbonic anhydrases. Biochem J 473:2023–2032
Supuran CT (2018) Carbonic anhydrases and metabolism. Metabolites 8: https://doi.org/10.3390/metabo8020025
Torres RJ, Cesar A, Pastor VA et al. (2015) A critical comparison of different approaches to sediment-quality assessments in the Santos Estuarine System in Brazil. Arch Environ Contam Toxicol 68:132–147. https://doi.org/10.1007/s00244-014-0099-2
Tripp BC, Smith K, Ferry JG (2001) Carbonic anhydrase: New insights for an ancient enzyme. J Biol Chem 276:48615–48618. https://doi.org/10.1074/jbc.R100045200
Vajreswari A, Rao PS, Kaplay SS, Tulpule PG (1983) Erythrocyte membrane in rats fed high erucic acid-containing mustard oil: Osmotic fragility, lipid composition, and (Na+, K+)- and (Ca2+, Mg2+)-ATPases. Biochem Med 29:74–84. https://doi.org/10.1016/0006-2944(83)90056-X
Vitale AM, Monserrat JM, Castilho P, Rodriguez EM (1999) Inhibitory effects of cadmium on carbonic anhydrase activity and ionic regulation of the estuarine crab Chasmagnathus granulata (decapoda, grapsidae). Comp Biochem Physiol - C Pharmacol Toxicol Endocrinol 122:121–129. https://doi.org/10.1016/S0742-8413(98)10094-4
Weis JS (2014) Physiological, developmental and behavioral effects of marine pollution. Springer Netherlands, Dordrecht
Wilbur KM (1964) Shell formation and regeneration. In: Physiology of Mollusca. Elsevier, pp 243–282
Wilbur KM, Saleuddin ASM (1983) Shell formation. In: The Mollusca. Elsevier, pp 235–287
Xuan M, Jia Y, Li J (2017) Reconstitution of motor protein ATPase. In: Li J (ed) Supramolecular Chemistry of Biomimetic Systems. Springer, Singapore, pp 237–258
Zebral YD, da Silva Fonseca J, Marques JA, Bianchini A (2019) Carbonic anhydrase as a biomarker of global and local impacts: Insights from calcifying animals. Int J Mol Sci 20:3092. https://doi.org/10.3390/ijms20123092
Acknowledgements
Authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), CAPES Foundation and National Council for Scientific and Technological Development (CNPq) for financial support and sponsorship.
Funding
This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Proc. n° 2015/25063-0). C.A.Y. Harayashiki and A.J. Luna were sponsored by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Proc. n° 2018/08015-0 and FAPESP Proc. n° 2019/23310-1, respectively). N. Gouveia was sponsored by CAPES foundation (Proc. no 88882.431091/2019-01) and I.B. Castro (PQ 302713/2018-2) was a research fellow of CNPq.
Author information
Authors and Affiliations
Contributions
Conceptualization: CAYH; Methodology: CAYH, HSH, LR deSB, NG, and AJL; Formal analysis and investigation: CAYH, HSH, LRde SB, NG, and AJL; Writing—original draft preparation: CAYH; Writing—review and editing: CAYH, HSH, LRde SB, NG, AO, and IBC; Funding acquisition: CAYH, IBC; Resources: AO.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Harayashiki, C.A.Y., Sadauskas-Henrique, H., de Souza-Bastos, L.R. et al. Contamination gradient affects differently carbonic anhydrase activity of mollusks depending on their feeding habits. Ecotoxicology 31, 124–133 (2022). https://doi.org/10.1007/s10646-021-02496-1
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-021-02496-1