title: Cellular effects of bacterial N-3-Oxo-dodecanoyl-L-Homoserine lactone on the sponge Suberites domuncula (Olivi, 1792): insights into an intimate inter-kingdom dialogue.
abstract: Sponges and bacteria have lived together in complex consortia for 700 million years. As filter feeders, sponges prey on bacteria. Nevertheless, some bacteria are associated with sponges in symbiotic relationships. To enable this association, sponges and bacteria are likely to have developed molecular communication systems. These may include molecules such as N-acyl-L-homoserine lactones, produced by Gram-negative bacteria also within sponges. In this study, we examined the role of N-3-oxododecanoyl-L-homoserine lactone (3-oxo-C12-HSL) on the expression of immune and apoptotic genes of the host sponge Suberites domuncula. This molecule seemed to inhibit the sponge innate immune system through a decrease of the expression of genes coding for proteins sensing the bacterial membrane: a Toll-Like Receptor and a Toll-like Receptor Associated Factor 6 and for an anti-bacterial perforin-like molecule. The expression of the pro-apoptotic caspase-like 3/7 gene decreased as well, whereas the level of mRNA of anti-apoptotic genes Bcl-2 Homolog Proteins did not change. Then, we demonstrated the differential expression of proteins in presence of this 3-oxo-C12-HSL using 3D sponge cell cultures. Proteins involved in the first steps of the endocytosis process were highlighted using the 2D electrophoresis protein separation and the MALDI-TOF/TOF protein characterization: α and β subunits of the lysosomal ATPase, a cognin, cofilins-related proteins and cytoskeleton proteins actin, α tubulin and α actinin. The genetic expression of some of these proteins was subsequently followed. We propose that the 3-oxo-C12-HSL may participate in the tolerance of the sponge apoptotic and immune systems towards the presence of bacteria. Besides, the sponge may sense the 3-oxo-C12-HSL as a molecular evidence of the bacterial presence and/or density in order to regulate the populations of symbiotic bacteria in the sponge. This study is the first report of a bacterial secreted molecule acting on sponge cells and regulating the symbiotic relationship.
authors.affiliation: Université de Bretagne-Sud, Laboratoire de Biotechnologie et de Chimie Marines, EA 3884, Institut Universitaire Européen de la Mer, Lorient, France.
authors.forename: Johan
authors.initials: J
authors.lastname: Gardères
authors.affiliation: Laboratoire des Mollusques Marins et des Ecosystèmes associés, CNRS INEE FRE 3484, Université de Caen Basse-Normandie, Caen, France.
authors.forename: Joël
authors.initials: J
authors.lastname: Henry
authors.affiliation: Post Genomic Platform PROTEOGEN, SF ICORE 4206, Université de Caen Basse-Normandie, Caen, France.
authors.forename: Benoit
authors.initials: B
authors.lastname: Bernay
authors.affiliation: Pontificia Universidad Católica de Chile - Departamento de Ecología Facultad de Ciencias Biológicas - Santiago - Chile.
authors.forename: Andrès
authors.initials: A
authors.lastname: Ritter
authors.affiliation: Laboratoire des Mollusques Marins et des Ecosystèmes associés, CNRS INEE FRE 3484, Université de Caen Basse-Normandie, Caen, France.
authors.forename: Céline
authors.initials: C
authors.lastname: Zatylny-Gaudin
authors.affiliation: European Research Council Advanced Investigator Grant Research Group at Institute for Physiological Chemistry, University Medical Center of the Johannes Gutenberg University, Mainz, Germany.
authors.forename: Matthias
authors.initials: M
authors.lastname: Wiens
authors.affiliation: European Research Council Advanced Investigator Grant Research Group at Institute for Physiological Chemistry, University Medical Center of the Johannes Gutenberg University, Mainz, Germany.
authors.forename: Werner E G
authors.initials: WE
authors.lastname: Müller
authors.affiliation: Université de Bretagne-Sud, Laboratoire de Biotechnologie et de Chimie Marines, EA 3884, Institut Universitaire Européen de la Mer, Lorient, France.
authors.forename: Gaël
authors.initials: G
authors.lastname: Le Pennec
mesh_terms: D015107:4-Butyrolactone / Q000031:analogs & derivatives* / Q000378:metabolism / Q000494:pharmacology; D000818:Animals; D017209:Apoptosis / Q000187:drug effects; D001419:Bacteria / Q000378:metabolism*; D004705:Endocytosis / Q000187:drug effects; D005786:Gene Expression Regulation / Q000187:drug effects; D006714:Homoserine / Q000031:analogs & derivatives* / Q000378:metabolism / Q000494:pharmacology; D007113:Immunity, Innate / Q000187:drug effects; D008565:Membrane Proteins / Q000378:metabolism; D011161:Porifera / Q000166:cytology / Q000187:drug effects* / Q000276:immunology / Q000382:microbiology*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D013559:Symbiosis
chemical_list: D008565:Membrane Proteins; C109860:N-(3-oxododecanoyl)homoserine lactone; D012333:RNA, Messenger; D006714:Homoserine; D015107:4-Butyrolactone