Sequence variability of the pattern recognition receptor Mermaid mediates specificity of marine nematode symbioses

• Published in: The ISME Journal Vol. 5; no. 6; pp. 986 - 998
• Main Authors: Bulgheresi, Silvia, Gruber-Vodicka, Harald R, Heindl, Niels R, Dirks, Ulrich, Kostadinova, Maria, Breiteneder, Heimo, Ott, Joerg A
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.06.2011; Oxford University Press; Nature Publishing Group
• Subjects: 631/158/2446/2447; 631/208/726/649; 631/250/262/2106; 631/326/2565/547; Amino Acid Sequence; Animals; Bacteria - classification; Bacteria - genetics; Bacteria - isolation & purification; Bacterial Physiological Phenomena; Biomedical and Life Sciences; Ecology; Evolutionary Biology; Helminth Proteins - chemistry; Life Sciences; Mannose-Binding Lectin - chemistry; Mannose-Binding Lectins - genetics; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Models, Molecular; Molecular Sequence Data; Nematoda - genetics; Nematoda - microbiology; Nematoda - physiology; Nematodes; Original; original-article; Pattern recognition; Phylogeny; Protein Isoforms - chemistry; Receptors, Pattern Recognition - chemistry; RNA, Ribosomal, 16S - genetics; Sequence Alignment; Shallow water; Sulfur; Symbiosis; marine sediment; microbe-associated molecular pattern receptor; nematode; symbiosis; sulfur-oxidizing bacteria; C-type lectin
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/ismej.2010.198

Selection of a specific microbial partner by the host is an all-important process. It guarantees the persistence of highly specific symbioses throughout host generations. The cuticle of the marine nematode Laxus oneistus is covered by a single phylotype of sulfur-oxidizing bacteria. They are embedded in a layer of host-secreted mucus containing the mannose-binding protein Mermaid. This Ca 2+ -dependent lectin mediates symbiont aggregation and attachment to the nematode. Here, we show that Stilbonema majum —a symbiotic nematode co-occurring with L. oneistus in shallow water sediment—is covered by bacteria phylogenetically distinct to those covering L. oneistus . Mermaid cDNA analysis revealed extensive protein sequence variability in both the nematode species. We expressed three recombinant Mermaid isoforms, which based on the structural predictions display the most different carbohydrate recognition domains (CRDs). We show that the three CRDs (DNT, DDA and GDA types) possess different affinities for L. oneistus and S. majum symbionts. In particular, the GDA type, exclusively expressed by S. majum , displays highest agglutination activity towards its symbionts and lowest towards its L. oneistus symbionts. Moreover, incubation of L. oneistus in the GDA type does not result in complete symbiont detachment, whereas incubation in the other types does. This indicates that the presence of particular Mermaid isoforms on the nematode surface has a role in the attachment of specific symbionts. This is the first report of the functional role of sequence variability in a microbe-associated molecular patterns receptor in a beneficial association.