Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes

Nussbaumer, Andrea D.; Bright, Monika; Baranyi, Christian; Beisser, Christian Josef; Ott, Jörg

doi:10.3354/ame034239

Cited by 31 publications

(14 citation statements)

References 45 publications

(35 reference statements)

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“…Whether the folliculinid ciliate depends on symbionts has not yet been demonstrated. However, symbioses form between ciliates and chemoautotrophic bacteria in other reducing environments (Bauer-Nebelsick et al 1996, Nussbaumer et al 2004, and the very depleted values found here for the folliculinid ciliate corroborate unpublished SEM observations of bacteria covering the surface of this ciliate (C.R.F. unpubl.…”

Section: Symbiont-bearing Faunasupporting

confidence: 89%

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Bergquist¹,

Eckner

Urcuyo³

et al. 2007

Mar. Ecol. Prog. Ser.

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To investigate food web structure in diffuse flow vent environments, an entire macrofaunal community associated with a single aggregation of the tubeworm Ridgeia piscesae was collected from a vent field on the Juan de Fuca Ridge in the NE Pacific. All members of the community were identified and enumerated, and the biomass and stable carbon (δ 13 C) and nitrogen (δ 15 N) isotope ratios were determined for almost all taxa. Symbiont-bearing invertebrates (primarily R. piscesae) accounted for a vast majority of the biomass of the community, and 3 presumably grazing bacterivorous gastropods dominated the biomass of the consumer fauna. Biomass and abundance of individuals declined from the bacterivore to the scavenger/detritivore to the predator feeding guild. Several species (a folliculinid ciliate, Idas washingtonia, Provanna variabilis) possessed unique stable isotope signatures, suggesting the possibility of symbiotic relationships with autotrophic bacteria. Stable isotope values varied widely between and occasionally within species in the lowest consumer levels suggesting a great diversity of food source 13 C and 15 N composition. Based on the distinct isotopic values of 3 bacterivores, 3 potential pools of isotopically-distinct microbial production were identified. The 4 highest-biomass predatory species (all polynoids) possessed δ 13 C and δ 15 N values consistent with a diet that included the tubeworm R. piscesae, a species comprising 83% of the total biomass in the collection, and the gastropod Depressigyra globulus, a species comprising 10% of the total biomass in the collection. A potential specialist predator (Clypeosectus curvus) on folliculinid ciliates was also identified. Overall the study suggested a dominant pattern of energy transfer from microbial producers to symbiont-bearing siboglinid tubeworms, various bacterivores (gastropods, polychaetes and pycnogonids), and detritivorous polychaetes to predaceous polynoids.

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Section: Symbiont-bearing Faunasupporting

confidence: 89%

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Bergquist¹,

Eckner

Urcuyo³

et al. 2007

Mar. Ecol. Prog. Ser.

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“…This result suggested a high specificity and the occurrence of an acute recognition mechanism such as in nematode ectosymbioses (Nussbaumer et al, 2004). Moreover, molecular surveys indicated a bacterial community switch occurring between the first stages of the R. exoculata life cycle (egg and hatched egg libraries dominated by the Gammaproteobacteria) and later stages (juvenile/adult libraries dominated by the Epsilonproteobacteria) (Table 1), confirmed by FISH observations (Figures 2a and b versus d).…”

Section: Epibiont Diversity and Acquisitionsupporting

confidence: 62%

Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata

et al. 2011

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The caridean shrimp Rimicaris exoculata dominates the fauna at several Mid-Atlantic Ridge hydrothermal vent sites. This shrimp has an enlarged gill chamber, harboring a dense ectosymbiotic community of chemoautotrophic bacteria associated with mineral oxide deposits. Until now, their acquisition is not fully understood. At three hydrothermal vent sites, we analyzed the epibionts diversity at different moult stages and also in the first stages of the shrimp life (eggs, hatched eggs (with larvae) and juveniles). Hatched eggs associated with young larvae were collected for the first time directly from gravid females at the Logachev vent site during the Serpentine cruise. An approach using 16S rRNA clone libraries, scanning and transmission electron microscopy, and fluorescent in situ hybridization was used. Molecular results and microscope observations indicated a switch in the composition of the bacterial community between early R. exoculata life cycle stage (egg libraries dominated by the Gammaproteobacteria) and later stages (juvenile/adult libraries dominated by the Epsilonproteobacteria). We hypothesized that the epibiotic phylotype composition could vary according to the life stage of the shrimp. Our results confirmed the occurrence of a symbiosis with Gammaproteobacteria and Epsilonproteobacteria, but more complex than previously assumed. We revealed the presence of active type-I methanotrophic bacteria colonizing the cephalothorax of shrimps from the Rainbow site. They were also present on the eggs from the Logachev site. This could be the first 'epibiotic' association between methanotrophic bacteria and hydrothermal vent crustacean. We discuss possible transmission pathways for epibionts linked to the shrimp life cycle.

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“…After 48 h, however, symbiontfree patches appeared on the worms, although the detached bacteria did not form visible aggregates in the surrounding media (data not shown). This may reflect the presence of free D-mannose, which is known to cause symbiont detachment, although with a much slower dynamic (i.e., dissociation starts only after 16 h and goes to completion after 90 h (22).…”

Section: Symbiont Binding To the Host Is Camentioning

confidence: 99%

“…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 symbionts by secreting a mannose-binding protein(s) from their posterior GSOs onto their cuticle.…”

mentioning

confidence: 91%

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

Bulgheresi

Schabussova

Chen

et al. 2006

Appl Environ Microbiol

103

105

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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...

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Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes

Cited by 31 publications

References 45 publications

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata

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

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