A New C-Type Lectin Similar to the Human Immunoreceptor DC-SIGN Mediates Symbiont Acquisition by a Marine Nematode

Abstract

Although thiotrophic symbioses have been intensively studied for the last three decades, nothing is known about the molecular mechanisms of symbiont acquisition. We used the symbiosis between the marine nematode Laxus oneistus and sulfur-oxidizing bacteria to study this process. In this association a monolayer of symbionts covers the whole cuticle of the nematode, except its anterior-most region. Here, we identify a novel Ca 2؉ -dependent mannose-specific lectin that was exclusively secreted onto the posterior, bacterium-associated region of L. oneistus cuticle. A recombinant form of this lectin induced symbiont aggregation in seawater and was able to compete with the native lectin for symbiont binding in vivo. Surprisingly, the carbohydrate recognition domain of this mannose-binding protein was similar both structurally and functionally to a human dendritic cell-specific immunoreceptor. Our results provide a molecular link between bacterial symbionts and host-secreted mucus in a marine symbiosis and suggest conservation in the mechanisms of host-microbe interactions throughout the animal kingdom.Stilbonematinae (Desmodoridae, Chromadoria) (27, 28) are especially abundant in tropical calcareous sands, where an oxidized surface layer overlies a reduced one. In the Belize Barrier Reef, two species, Laxus oneistus and Stilbonema majum, even dominate the nematode fauna of shallow sands. Stilbonematids repeatedly cross the boundary between oxidized and reduced sediment layers and thus represent an ideal substrate for bacteria that require both oxygen and sulfide. The worms, in turn, appear to obtain most of their nutrition by grazing on their symbionts (29).Another peculiar feature of symbiotic marine nematodes is a conspicuous system of glandular sensory organs (GSOs) underlying their cuticle (see Fig. 2D). The GSOs produce a mucus envelope in which symbionts may be embedded. In each GSO the secretory granules accumulate in the canal and are released onto the cuticle surface through a hollow seta (18,19).There is no evidence of vertical transmission of the symbionts, but even very small juveniles carry a complete microbial coat. Colonization of recently hatched or molted stilbonematids must be a rapid process because field collections rarely yielded nonsymbiotic stilbonematids.In L. oneistus, whose bacterial coat is composed of a single phylotype of rod-shaped ␥-Proteobacteria (26, 31, 30), symbiont recruitment must be highly selective. The microbial coat starts with a sharp onset some distance behind the anterior end, and the bacterial rods are aligned perpendicularly to the worm's surface. The absence of symbionts on the anterior region does not correlate with fewer or smaller GSOs or with reduced mucus production.Incubation in D-mannose specifically led to symbiont detachment from nematodes belonging to the genus Laxus but not from S. majum. Furthermore, this monosaccharide was found on the surface of the symbionts, but not on L. oneistus cuticle (22). These data led to the hypothesis that L. oneistus binds its s...

Human Dendritic Cell-Specific Intercellular Adhesion Molecule-Grabbing Nonintegrin (CD209) Is a Receptor forYersinia pestisThat Promotes Phagocytosis by Dendritic Cells

“…The carbohydrate recognition domain of Mermaid shares both structural and functional similarity with that of DC-SIGN as described previously (9). A recombinant form of Mermaid (His-Mermaid) was expressed and purified as described previously (9).…”

Role of N-Acetylglucosamine within Core Lipopolysaccharide of Several Species of Gram-Negative Bacteria in Targeting the DC-SIGN (CD209)

“…However, DC-SIGN is a transmembrane protein and it is possible that purified DC-SIGN will not retain its biological functions. Recently, we contributed to the identification of Mermaid, a marine nematode Ca 2ϩ -dependent lectin whose carbohydrate recognition domain shares both structural and functional similarity with that of DC-SIGN (48). Therefore, we tested the ability of a recombinant form of Mermaid to bind CS180, thereby inhibiting the core LPS-DC-SIGN interaction.…”

“…It is expected that the interaction of Mermaid with bacteria induces symbiont aggregation in seawater leading to symbiosis (48). His-Mermaid was expressed and purified as described previously (48). FITC-conjugated His-Mermaid (FITC-His-Mermaid) was obtained with the FITC Labeling kit (Calbiochem) according to the manufacturer's instructions.…”

“…Recently, Mermaid has been identified as a DC-SIGN-like protein. It is expected that the interaction of Mermaid with bacteria induces symbiont aggregation in seawater leading to symbiosis (48). His-Mermaid was expressed and purified as described previously (48).…”

High Affinity Interaction between a Bivalve C-type Lectin and a Biantennary Complex-type N-Glycan Revealed by Crystallography and Microcalorimetry

“…For example, lectins play a role in aggregation mechanisms in corals and sponges (3) or in sperm-egg recognition in oysters (4). Lectin mediation of symbiosis with algae or bacteria has been observed in coral (5) and nematodes (6). Nevertheless, the most common function assessed for lectins in marine invertebrates is their role in innate immunity by specific binding of polysaccharide-coated pathogenic bacteria (7,8).…”