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

ABSTRACT: 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.

SUBMITTER: Bulgheresi S

PROVIDER: S-EPMC3131856 | biostudies-literature | 2011 Jun

REPOSITORIES: biostudies-literature

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

Bulgheresi Silvia S Gruber-Vodicka Harald R HR Heindl Niels R NR Dirks Ulrich U Kostadinova Maria M Breiteneder Heimo H Ott Joerg A JA

The ISME journal 20110113 6

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 Stilbo ...[more]

PMID: 21228893

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Project description:Eukaryotes may experience oxygen deprivation under several physiological and pathological conditions. Because oxygen shortage leads to a reduction in cellular energy production, all the eukaryotes studied so far evolved ways to conserve energy via suppression of metabolism. However, the molecular physiology of animals that naturally and repeatedly experience anoxia is poorly studied. One such animal is the symbiotic marine nematode Laxus oneistus. This thrives, invariably coated by its sulfur-oxidizing bacterium Candidatus Thiosymbion oneisti, in anoxic sulfidic or hypoxic sand. Here, by applying transcriptomics and proteomics, we discovered that, irrespective of the oxygen concentration it is subjected to, this nematode is mostly and constitutively engaging in ubiquitination-mediated proteolysis, energy generation, oxidative stress response and immune response. Furthermore, by incubating L. oneistus under sulfidic anoxic or hypoxic conditions, we found that, under the first condition, the worm upregulated genes involved in ribosome biogenesis, proteolytic systems (autophagy and the ubiquitin-proteasome system), chaperones, detoxification and lectins. Degradation pathways were likely induced to recycle damaged cellular components (mitochondria) and misfolded proteins into nutrients, whereas lectins were likely expressed to promote the attachment of its anaerobic, thiotrophic symbiont. Besides, L. oneistus appeared to survive oxygen deprivation by using alternative electron carriers (rhodoquinone) and acceptors (fumarate) to rewire the electron transfer chain. On the other hand, under hypoxia, genes involved in costly processes (e.g., development, amino acid biosynthesis, feeding behaviour, mating) were upregulated. Intriguingly, the worm’s Toll-like innate immunity pathway and a number of immune effectors (e.g., Bacterial Permeability Increasing proteins, fungicides) were upregulated in the presence of oxygen. In conclusion, we hypothesize that L. oneistus survives in anoxic sulfidic sand by overexpressing degradation processes, rewiring oxidative phosphorylation and by reinforcing its coat of bacterial sulfur-oxidizers. In the presence of oxygen, instead, it appears to exploit glycolysis to eat, mate and grow. Moreover, oxygen appears to affect L. oneistus immune system in such way, as to favor specific attachment of its anaerobic partner in anoxia and to produce broad-range antimicrobials when oxygen is present.

Dataset Information

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

Publications

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

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