Density of Compatible Ligands on the Surface of Food Particles Modulates Sorting Efficiency in the Blue Mussel Mytilus edulis

The adhesion between food particles and mucus is a fundamental process in particle sorting in suspension-feeding bivalves that requires specific recognition. Interactions between carbohydrate-binding proteins (lectins) expressed on the feeding organs and carbohydrates present on microbial cell surface can provide this specificity. Microalga cell surface carbohydrates (MCSC) represent unique patterns that can be considered as species-specific fingerprints. In this study, sorting efficiencies in blue mussels Mytilus edulis fed with microalgae having modified MCSC and engineered microspheres coated with target carbohydrates was measured. The nature and quantities of surface carbohydrates required to trigger sorting in mussels was evaluated and the relationship between ligand quantities and sorting efficiency (SE) was determined. Mussels fed with Chlamydomonas which MCSC were blocked with ConA or PEA lectins (affinity to mannose and glucose) led to a significant decrease of the sorting efficiencies, not observed when the lectin UEA (affinity to fucose) was used. The ability of commercial lectins to inhibit sorting was not linear and a threshold was noted between 30 and 45 ug lectins per million algae cells. Further, mussels were fed with microspheres coated with neoglycoproteins. Results showed that glucose-BSA, but not fucose-BSA, has an effect on particle sorting in mussels, and 1.08 x 109 molecules of glucose per microspheres, corresponding to a density of 6.99 x 106 molecules of glucose per µm2, triggers particle selection. These findings support that selection of food particles by mussels rely on the strength of the bond between suspended particle and the mucosal layer that mediate sorting, and that these bonds depend on the quantity of compatible ligands on each particle.

[1]  B. Allam,et al.  Particle Selection in Suspension-Feeding Bivalves: Does One Model Fit All? , 2020, The Biological Bulletin.

[2]  B. Allam,et al.  Reverse genetics demonstrate the role of mucosal C-type lectins in food particle selection in the oyster Crassostrea virginica , 2018, Journal of Experimental Biology.

[3]  Ajit Varki,et al.  Biological roles of glycans , 2016, Glycobiology.

[4]  Yan Shi,et al.  Variation in Carbohydrates between Cancer and Normal Cell Membranes Revealed by Super‐Resolution Fluorescence Imaging , 2016, Advanced science.

[5]  G. Wikfors,et al.  Modeling food choice in the two suspension-feeding bivalves, Crassostrea virginica and Mytilus edulis , 2016 .

[6]  B. Allam,et al.  Food quality and season affect gene expression of the mucosal lectin MeML and particle sorting in the blue mussel Mytilus edulis , 2013 .

[7]  J. Samitier,et al.  Cell adhesion and focal contact formation on linear RGD molecular gradients: study of non-linear concentration dependence effects. , 2012, Nanomedicine : nanotechnology, biology, and medicine.

[8]  G. Boons,et al.  Carbohydrate recognition : biological problems, methods, and applications , 2011 .

[9]  Caifeng Ding,et al.  Electrochemical cytosensor based on gold nanoparticles for the determination of carbohydrate on cell surface. , 2011, Analytical biochemistry.

[10]  B. Allam,et al.  Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica. , 2011, Fish & shellfish immunology.

[11]  B. Allam,et al.  Identification and molecular characterization of a mucosal lectin (MeML) from the blue mussel Mytilus edulis and its potential role in particle capture. , 2010, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[12]  Gary S. Caldwell,et al.  Marine Glycobiology: Current Status and Future Perspectives , 2010, Marine Biotechnology.

[13]  Jun‐Jie Zhu,et al.  Design and implementation of electrochemical cytosensor for evaluation of cell surface carbohydrate and glycoprotein. , 2010, Analytical chemistry.

[14]  S. Shumway,et al.  Lectins Associated With the Feeding Organs of the Oyster Crassostrea virginica Can Mediate Particle Selection , 2009, The Biological Bulletin.

[15]  D. Allemand,et al.  Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms , 2009, BMC Physiology.

[16]  B. Allam,et al.  Particle selection in the ribbed mussel Geukensia demissa and the Eastern oyster Crassostrea virginica: Effect of microalgae growth stage , 2008 .

[17]  H. Ju,et al.  Effective cell capture with tetrapeptide-functionalized carbon nanotubes and dual signal amplification for cytosensing and evaluation of cell surface carbohydrate. , 2008, Analytical chemistry.

[18]  Lizhen Lin,et al.  Fourteen FITC-conjugated lectins as a tool for the recognition and differentiation of some harmful algae in Chinese coastal waters , 2008, Journal of Applied Phycology.

[19]  B. Ji,et al.  Nonlinear mechanical modeling of cell adhesion. , 2008, Journal of theoretical biology.

[20]  V. Weis,et al.  Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis , 2006, Cellular microbiology.

[21]  B. Allam,et al.  Comparative Growth and Survival of Juvenile Hard Clams, Mercenaria mercenaria, Fed Commercially Available Diets , 2006 .

[22]  N. Sharon,et al.  History of lectins: from hemagglutinins to biological recognition molecules. , 2004, Glycobiology.

[23]  A. Engel,et al.  Carbohydrate–carbohydrate interaction provides adhesion force and specificity for cellular recognition , 2004, The Journal of Cell Biology.

[24]  E. Cho Cluster analysis on the lectin binding patterns of marine microalgae , 2003 .

[25]  M. Sakaguchi,et al.  Involvement of a 40-kDa glycoprotein in food recognition, prey capture, and induction of phagocytosis in the protozoon Actinophrys sol. , 2001, Protist.

[26]  M. Ucko,et al.  GLYCOPROTEIN MOIETY IN THE CELL WALL OF THE RED MICROALGA PORPHYRIDIUM SP. (RHODOPHYTA) AS THE BIORECOGNITION SITE FOR THE CRYPTHECODINIUM COHNII‐LIKE DINOFLAGELLATE , 1999 .

[27]  P. Stahl,et al.  The mannose receptor is a pattern recognition receptor involved in host defense. , 1998, Current opinion in immunology.

[28]  S. Benoff Carbohydrates and fertilization: an overview. , 1997, Molecular human reproduction.

[29]  C. Wong,et al.  Intervention of carbohydrate recognition by proteins and nucleic acids. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  A. Varki,et al.  Biological roles of oligosaccharides: all of the theories are correct , 1993, Glycobiology.

[31]  L. Fritz,et al.  Gamete recognition during fertilization in a red alga,Antithamnion nipponicum , 1993, Protoplasma.

[32]  E. Navarro,et al.  Feeding, particle selection and absorption in cockles Cerastoderma edule (L.) exposed to variable conditions of food concentration and quality , 1992 .

[33]  P. G. Allen,et al.  Phagocytosis in Acanthamoeba: I. A mannose receptor is responsible for the binding and phagocytosis of yeast , 1990, Journal of cellular physiology.

[34]  V. Loosanoff,et al.  Feeding of Oysters in Relation to Density of Microorganisms. , 1947, Science.

[35]  C. M. Martel Conceptual Bases for Prey Biorecognition and Feeding Selectivity in the Microplanktonic Marine Phagotroph Oxyrrhis marina , 2008, Microbial Ecology.

[36]  D. H. Jones,et al.  Biochemical prey recognition by planktonic protozoa. , 2007, Environmental microbiology.

[37]  M. Burger,et al.  Circular proteoglycans from sponges: first members of the spongican family , 2003, Cellular and Molecular Life Sciences CMLS.

[38]  J. Prou,et al.  Particle selection in the oyster Crassostrea gigas (Thunberg) studied by pigment HPLC analysis under natural food conditions , 1996 .

[39]  R. Newell,et al.  Preferential ingestion of organic material by the American oyster Crassostrea virginica , 1983 .

[40]  R. Guillard,et al.  Culture of Phytoplankton for Feeding Marine Invertebrates , 1975 .