Detection of the Free-Living Forms of Sulfide-Oxidizing Gill Endosymbionts in the Lucinid Habitat (
            <i>Thalassia testudinum</i>
            Environment)

Gros, Olivier; Liberge, Martine; Heddi, Abdelaziz; Khatchadourian, Chaqué; Felbeck, Horst

doi:10.1128/aem.69.10.6264-6267.2003

Cited by 46 publications

(34 citation statements)

References 39 publications

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“…The C. orbicularis symbiont exists as a free-living bacterium in the environment before colonization of its bivalve host 9 and therefore presumably belongs to this microbial seagrass community. Moreover, free-living sulfide oxidizers are known to be part of the complex bacterial population in the seagrass rhizosphere ( Supplementary Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The shallowwater lucinid Codakia orbicularis, which lives in the sediment beneath the tropical seagrass Thalassia testudinum along the Caribbean and Western Atlantic coast 5 , harbours a single species of endosymbionts in its gills 6 . The symbiont has been shown to be newly acquired by each clam generation 7,8 from a pool of freeliving symbiosis-competent bacteria in the environment 9 , rather than being inherited from clam parents. C. orbicularis appears not to release its endosymbionts, even under adverse conditions, but can digest them as a source of nutrition [10][11][12] .…”

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Nitrogen fixation in a chemoautotrophic lucinid symbiosis

et al. 2016

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The shallow water bivalve Codakia orbicularis lives in symbiotic association with a sulfur-oxidizing bacterium in its gills. The endosymbiont fixes CO 2 and thus generates organic carbon compounds, which support the host's growth. To investigate the uncultured symbiont's metabolism and symbiont-host interactions in detail we conducted a proteogenomic analysis of purified bacteria. Unexpectedly, our results reveal a hitherto completely unrecognized feature of the C. orbicularis symbiont's physiology: the symbiont's genome encodes all proteins necessary for biological nitrogen fixation (diazotrophy). Expression of the respective genes under standard ambient conditions was confirmed by proteomics. Nitrogenase activity in the symbiont was also verified by enzyme activity assays. Phylogenetic analysis of the bacterial nitrogenase reductase NifH revealed the symbiont's close relationship to free-living nitrogen-fixing Proteobacteria from the seagrass sediment. The C. orbicularis symbiont, here tentatively named 'Candidatus Thiodiazotropha endolucinida', may thus not only sustain the bivalve's carbon demands. C. orbicularis may also benefit from a steady supply of fixed nitrogen from its symbiont-a scenario that is unprecedented in comparable chemoautotrophic symbioses. Mutualistic associations between marine invertebrates and sulfur-oxidizing (thiotrophic) bacteria are a well-documented and widespread phenomenon in a variety of sulfidic habitats ranging from hydrothermal vents to shallow-water coastal ecosystems 1-3 . Thioautotrophic symbionts generate energy through sulfide oxidation and provide their hosts with organic carbon. In the Lucinidae, a diverse family of marine bivalves, all members are obligatorily dependent on their bacterial gill endosymbionts after larval development and metamorphosis 4 . The shallowwater lucinid Codakia orbicularis, which lives in the sediment beneath the tropical seagrass Thalassia testudinum along the Caribbean and Western Atlantic coast 5 , harbours a single species of endosymbionts in its gills 6 . The symbiont has been shown to be newly acquired by each clam generation 7,8 from a pool of freeliving symbiosis-competent bacteria in the environment 9 , rather than being inherited from clam parents. C. orbicularis appears not to release its endosymbionts, even under adverse conditions, but can digest them as a source of nutrition [10][11][12] . Moreover, bacterial cell division seems to be inhibited inside the host tissue. The majority of the symbiont population was shown to be polyploid (that is, containing multiple genome copies), while dividing symbiont cell stages are very rarely observed in host bacteriocytes 13 . The host undoubtedly benefits from the symbiont both by way of detoxification of its sulfidic environment and by supply of organic compounds through the bacterial Calvin-Benson cycle. It remains questionable, however, whether the symbiont gains any advantage from this association in evolutionary terms 11 .Biological nitrogen fixation (diazotrophy) is the conversion of ...

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Nitrogen fixation in a chemoautotrophic lucinid symbiosis

et al. 2016

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“…The direct detection of the tube worm symbiont in biofilms supports the hypothesis that these bacteria exist in the free-living vent environment. Indeed, in a coastal marine endosymbiosis, the 16S phylotype of bacterial symbionts of Codakia orbicularis clams is readily found in the sea grass sediment surrounding their hosts (11).…”

Section: Sample Collectionmentioning

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Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Harmer

Rotjan

Nussbaumer

et al. 2008

Appl Environ Microbiol

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Recent evidence suggests that deep-sea vestimentiferan tube worms acquire their endosymbiotic bacteria from the environment each generation; thus, free-living symbionts should exist. Here, free-living tube worm symbiont phylotypes were detected in vent seawater and in biofilms at multiple deep-sea vent habitats by PCR amplification, DNA sequence analysis, and fluorescence in situ hybridization. These findings support environmental transmission as a means of symbiont acquisition for deep-sea tube worms.

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“…gouldi habitat, we first used fluorescence in situ hybridization (FISH) to label bacteria extracted from sediment samples, as in (Gros et al, 2003). Based on the 16S rRNA sequence obtained, a 20-base oligonucleotide probe specific for T. cf.…”

Section: Detection Of Free-living Symbionts In Sedimentsmentioning

confidence: 99%

Magnetosome-containing bacteria living as symbionts of bivalves

et al. 2014

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Bacteria containing magnetosomes (protein-bound nanoparticles of magnetite or greigite) are common to many sedimentary habitats, but have never been found before to live within another organism. Here, we show that octahedral inclusions in the extracellular symbionts of the marine bivalve Thyasira cf. gouldi contain iron, can exhibit magnetic contrast and are most likely magnetosomes. Based on 16S rRNA sequence analysis, T. cf. gouldi symbionts group with symbiotic and free-living sulfur-oxidizing, chemolithoautotrophic gammaproteobacteria, including the symbionts of other thyasirids. T. cf. gouldi symbionts occur both among the microvilli of gill epithelial cells and in sediments surrounding the bivalves, and are therefore facultative. We propose that free-living T. cf. gouldi symbionts use magnetotaxis as a means of locating the oxic-anoxic interface, an optimal microhabitat for chemolithoautotrophy. T. cf. gouldi could acquire their symbionts from near-burrow sediments (where oxic-anoxic interfaces likely develop due to the host's bioirrigating behavior) using their superextensile feet, which could transfer symbionts to gill surfaces upon retraction into the mantle cavity. Once associated with their host, however, symbionts need not maintain structures for magnetotaxis as the host makes oxygen and reduced sulfur available via bioirrigation and sulfur-mining behaviors. Indeed, we show that within the host, symbionts lose the integrity of their magnetosome chain (and possibly their flagellum). Symbionts are eventually endocytosed and digested in host epithelial cells, and magnetosomes accumulate in host cytoplasm. Both host and symbiont behaviors appear important to symbiosis establishment in thyasirids.

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Detection of the Free-Living Forms of Sulfide-Oxidizing Gill Endosymbionts in the Lucinid Habitat ( Thalassia testudinum Environment)

Cited by 46 publications

References 39 publications

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Magnetosome-containing bacteria living as symbionts of bivalves

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