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Giant peroxisomes revealed by a comparative microscopy study of digestive gland cells of cephalaspidean sea slugs (Gastropoda, Euopisthobranchia)

Published online by Cambridge University Press:  20 November 2017

Alexandre Lobo-da-Cunha ,
Elsa Oliveira ,
Ângela Alves  and
Gonçalo Calado
Alexandre Lobo-da-Cunha*
Affiliation:
Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), 4450-208 Matosinhos, Portugal
Elsa Oliveira
Affiliation:
Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal
Ângela Alves
Affiliation:
Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4050-313 Porto, Portugal
Gonçalo Calado
Affiliation:
Department of Life Sciences, Lusophone University of Humanities and Technologies, 1749-024 Lisbon, Portugal
*
Correspondence should be addressed to: A. Lobo da Cunha, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar, Rua Jorge Viterbo Ferreira 228, 4050-313 Porto, Portugal email: alcunha@icbas.up.pt
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Abstract

Peroxisomes are cytoplasmic organelles involved in fatty acid oxidation, ether-phospholipids biosynthesis, glyoxylate metabolism and purine catabolism among other metabolic pathways. However, these organelles are still poorly studied in molluscs. During a light and electron microscopy study of the digestive glands of cephalaspidean sea slugs unusually large peroxisomes reaching about 5 µm in diameter were found in basophilic cells of Philinopsis depicta (Aglajidae), being among the biggest ever reported in metazoan cells. These round or oval peroxisomes were clearly visible with the light microscope, and their diamond shaped core was strongly stained by the tetrazonium coupling reaction for protein detection. However, in the basophilic cells of Aglaja tricolorata, another aglajid cephalaspidean, peroxisomes were more variable in shape and no bigger than 1 µm in length. Round peroxisomes with a diameter of about 0.5 µm were common in basophilic cells of Philine quadripartita (Philinidae) and Haminoea navicula (Haminoidae), whereas in Bulla striata (Bullidae) these organelles frequently had a diameter of between 1.0 and 1.5 µm. Peroxisomes were larger in basophilic cells than in digestive ones. In all these species, the electron-dense peroxisomal cores were diamond-shaped, and in H. navicula two cores could be seen in each peroxisome. The abundance and large size of peroxisomes in the digestive gland points out the importance of these organelles in the metabolism of this organ.

Keywords

Cephalaspideadigestive glandmolluscsperoxisomesTEMultrastructure
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 1 , February 2019 , pp. 197 - 202
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Beard, M.E. and Holtzman, E. (1985) Peroxisomes in the nervous system of Aplysia californica: a cytochemical study. Journal of Neurocytology 14, 513–524.Google Scholar
Bolte, K., Rensing, S.A. and Maier, U.-G. (2015) The evolution of eukaryotic cells from the perspective of peroxisomes: phylogenetic analyses of peroxisomal beta-oxidation enzymes support mitochondria-first models of eukaryotic cell evolution. Bioessays 37, 195–203.Google Scholar
Cajaraville, M.P., Cancio, I., Ibabe, A. and Orbea, A. (2003) Peroxisome proliferation as a biomarker in environmental pollution assessment. Microscopy Research and Technique 61, 191–202.Google Scholar
Cajaraville, M.P., Völkl, A. and Fahimi, H.D. (1992) Peroxisomes in the digestive gland cells of the mussel Mytilus galloprovincialis Lmk. Biochemical, ultrastructural and immunocytochemical characterization. European Journal of Cell Biology 56, 255–264.Google Scholar
Cancio, I. and Cajaraville, M.P. (2000) Cell biology of peroxisomes and their characteristics in aquatic organisms. International Review of Cytology 199, 201–293.Google Scholar
Cancio, I., Ibabe, A. and Cajaravile, P.M. (1999) Seasonal variation of peroxisomal enzyme activities and peroxisomal structure in mussels Mytilus galloprovincialis and its relationship with the lipid content. Comparative Biochemistry and Physiology C 123, 135–144.Google Scholar
Cancio, I., Völkl, A., Beier, K., Fahimi, H.D. and Cajaraville, M.P. (2000) Peroxisomes in molluscs, characterization by subcellular fractionation combined with western blotting, immunohistochemistry, and immunocytochemistry. Histochemistry and Cell Biology 113, 51–60.Google Scholar
Dannen, E. and Beard, M.E. (1977) Peroxisomes in pulmonate gastropods. Journal of Histochemistry and Cytochemistry 25, 319–328.Google Scholar
Dimitriadis, V.K. and Andrews, E.B. (2000) Ultrastructural and cytochemical study of the digestive gland cells of the marine prosobranch Nucella lapillus (L.) in relation to function. Malacologia 42, 103–112.Google Scholar
Gabaldón, T. (2010) Peroxisome diversity and evolution. Philosophical Transactions of the Royal Society B 365, 765–773.Google Scholar
Hartmann, H., Hess, M. and Haszprunar, G. (2011) Interactive 3D anatomy and affinities of Bathysciadiidae (Gastropoda, Cocculinoidea): deep-sea limpets feeding on decaying cephalopod beaks. Journal of Morphology 272, 259–279.Google Scholar
Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R.T., Reumann, S. and Zolmanh, B.K. (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279–2303.Google Scholar
Islinger, M., Cardoso, M.J.R. and Schrader, M. (2010) Be different – the diversity of peroxisomes in the animal kingdom. Biochimica et Biophysica Acta 1803, 881–897.Google Scholar
Lobo-da-Cunha, A. (1997) The peroxisomes of the hepatopancreas in two species of chitons. Cell and Tissue Research 290, 655–664.Google Scholar
Lobo-da-Cunha, A. (1999) Ultrastructural and cytochemical aspects of the basophilic cells in the hepatopancreas of Aplysia depilans (Mollusca, Opistobranchia). Tissue and Cell 31, 8–16.Google Scholar
Lobo-da-Cunha, A. (2000) The digestive cells of the hepatopancreas in Aplysia depilans (Mollusca, Opisthobranchia): ultrastructural and cytochemical study. Tissue and Cell 32, 49–57.Google Scholar
Lobo-da-Cunha, A., Alves, A., Oliveira, E. and Calado, G. (2016) Comparative study of salivary glands in carnivorous and herbivorous cephalaspideans (Gastropoda: Euopisthobranchia). Journal of Molluscan Studies 82, 43–54.Google Scholar
Lobo-da-Cunha, A., Batista, C. and Oliveira, E. (1994) The peroxisomes of the hepatopancreas in marine gastropods. Biology of the Cell 82, 67–74.Google Scholar
Lobo-da-Cunha, A., Malheiro, A.R., Alves, A., Oliveira, E., Coelho, R. and Calado, R. (2011a) Histological and ultrastructural characterisation of the stomach and intestine of the opisthobranch Bulla striata (Heterobranchia: Cephalaspidea). Thalassas 27, 61–75.Google Scholar
Lobo-da-Cunha, A., Oliveira, E., Alves, A., Coelho, R. and Calado, G. (2010a) Light and electron microscopic study of the anterior esophagus of Bulla striata (Mollusca, Opisthobranchia). Acta Zoologica 91, 125–138.Google Scholar
Lobo-da-Cunha, A., Oliveira, E., Ferreira, I., Coelho, R. and Calado, G. (2010b) Histochemical and ultrastructural characterization of the posterior esophagus of Bulla striata (Mollusca, Opisthobranchia). Microscopy and Microanalysis 16, 688–698.Google Scholar
Lobo-da-Cunha, A., Pereira-Sousa, J., Oliveira, E., Alves, A., Guimarães, F. and Calado, G. (2014) Calcium detection and other cellular studies in the esophagus and crop of the marine slug Aglaja tricolorata (Euopisthobranchia, Cephalaspidea). Malacologia 57, 365–376.Google Scholar
Lobo-da-Cunha, A., Santos, T., Oliveira, E., Alves, A., Coelho, R. and Calado, G. (2011b) Microscopical study of the crop and oesophagus of the carnivorous opisthobranch Philinopsis depicta (Cephalaspidea, Aglajidae). Journal of Molluscan Studies 77, 322–331.Google Scholar
Luchtel, D.L., Martin, A.W., Deyrup-Olsen, I. and Boer, H.H. (1997) Gastropoda: Pulmonata. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates, Volume 6B. New York, NY: Wiley-Liss, pp. 459–718.Google Scholar
Malaquias, M.A.E., Bericibar, E. and Reid, D.G. (2009) Reassessment of the trophic position of Bullidae (Gastropoda: Cephalaspidea) and the importance of diet in the evolution of cephalaspidean gastropods. Journal of Zoology 227, 88–97.Google Scholar
Malik, Z., Jones, C.J.P. and Connock, M.J. (1987) Assay and subcellular localization of H2O2 generating mannitol oxidase in the terrestrial slug Arion ater. Journal of Experimental Zoology 242, 9–15.Google Scholar
Orbea, A., Beier, K., Völkl, A., Fahimi, H.D. and Cajaraville, M.P. (1999) Ultrastructural, immunocytochemical and morphometric characterization of liver peroxisomes in gray mullet, Mugil cephalus L. Cell and Tissue Research 297, 493–502.Google Scholar
Oskars, T.R., Bouchet, P. and Malaquias, M.A.E. (2015) A new phylogeny of the Cephalaspidea (Gastropoda: Heterobranchia) based on expanded taxon sampling and gene markers. Molecular Phylogenetics and Evolution 89, 130–150.Google Scholar
Owen, G. (1972) Peroxisomes in the digestive diverticula of the bivalve mollusc Nucula sulcata. Zeitschrift für Zellforschung und Mikroskopische Anatomie 132, 15–24.Google Scholar
Oxford, G.S. (1977) Multiple sources of esterase enzymes in the crop juice of Cepaea (Mollusca: Helicidae). Journal of Comparative Physiology 122, 375–383.Google Scholar
Oxford, G.S. (1979) The subcellular localisation of certain crop-juice esterases in the digestive gland of Cepaea (Mollusca: Helicidae). Journal of Comparative Physiology 132, 327–335.Google Scholar
Pierce, S.K. and Curtis, N.E. (2012) The cell biology of the chloroplast symbiosis in sacoglossan sea slugs. International Review of Cell and Molecular Biology 293, 123–148.Google Scholar
Rocha, E., Lobo-da-Cunha, A., Monteiro, R.A.F., Silva, M.W. and Oliveira, M.H. (1999) A stereological study along the year on the hepatocytic peroxisomes of brown trout (Salmo trutta). Journal of Submicroscopic Cytology and Pathology 31, 91–105.Google Scholar
Sibirny, A.A. (2016) Yeast peroxisomes: structure, functions and biotechnological opportunities. FEMS Yeast Research 16, fow028.Google Scholar
Smith, J.J. and Aitchison, J.D. (2013) Peroxisomes take shape. Nature Reviews Molecular Cell Biology 14, 803–817.Google Scholar
Stewart, J.M., Carlin, R.C., Macdonald, J.A. and Van Iderstine, S. (1994) Fatty acid binding proteins and fatty acid catabolism in marine invertebrates: peroxisomal β-oxidation. Invertebrate Reproduction and Development 25, 73–82.Google Scholar
Taïeb, N. (2001) Distribution of digestive tubules and fine structure of digestive cells of Aplysia punctata (Cuvier, 1803). Journal of Molluscan Studies 67, 169–182.Google Scholar
Vamecq, J., Cherkaoui-Malki, M., Andreoletti, P. and Latruffe, N. (2014) The human peroxisome in health and disease: the story of an oddity becoming a vital organelle. Biochimie 98, 4–15.Google Scholar
Völkl, A., Baumgart, E. and Fahimi, H.D. (1988) Localization of urate oxidase in the crystalline cores of rat liver peroxisomes by immunocytochemistry and immunoblotting. Journal of Histochemistry and Cytochemistry 36, 329–336.Google Scholar
Voltzow, J. (1994) Gastropoda: Prosobranchia. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates, Volume 5. New York, NY: Wiley-Liss, pp. 111–252.Google Scholar
Wägele, H., Klussmann-Kolb, A., Verbeek, E. and Schrödle, M. (2014) Flashback and foreshadowing – a review of the taxon Opisthobranchia. Organism Diversity and Evolution 14, 133–149.Google Scholar
Zamora-Silva, A. and Malaquias, M.A.E. (2016) Diet preferences of the Aglajidae: a family of cephalaspidean gastropod predators on tropical and temperate shores. Journal of the Marine Biological Association of the United Kingdom 96, 1101–1112.Google Scholar