Significance of the occurrence of chemoautotrophic bacterial endosymbionts in lucinid clams from Bermuda

Schweimanns, M.; Felbeck, Horst

doi:10.3354/meps024113

Cited by 72 publications

(26 citation statements)

References 23 publications

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“…Species that have been analysed for their stable carbon isotope composition all show unusual ratios of 13C to 12C, from which it has been inferred that much of the carbon in the host tissues is supplied by the bacteria and thus derived from autotrophically-fixed CO2 (Rau & Hedges 1979, Rau 1981, Williams et al 1981, Felbeck 1983. Other invertebrates, more widely distributed in shelf and slope sediments, are now known to contain autotrophic endosymbiotic bacteria , Dando et al 1985, Schweimanns & Felbeck 1985 and several of them can exist in habitats where the dissolved suphide concentration is C 1 @ l (Dando et al 1985). The first report of stable carbon isotope ratios in symbiont-containing animals from habitats not rich in dissolved sulphide ) concerned 3 small species of gutless Pogonophora, whose tissues were extremely depleted in 13C when compared with heterotrophic benthic invertebrates and with particulate organic carbon from the habitat.…”

Section: Introductionmentioning

confidence: 99%

13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutricional importance of chemoautotrophic endosymbiotic bacteria

Spiro¹,

Greenwood²,

Southward³

et al. 1986

Mar. Ecol. Prog. Ser.

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The carbon isotope composition (6l3C%0) of the tissues of benthic invertebrates usually ranges from -16 to -20. In contrast we report that several common bivalve molluscs belonging to the superfamily Lucinacea and several small species of Pogonophora show much greater depletions, ranging from -23 to -31 in the bivalves and from -35 to -46 in the pogonophores. These bivalves and pogonophores live in reducing sediments where the concentration of dissolved sulphide is low, usually < 1 PM. The gills of the bivalves and the trophosome tissue of the pogonophores contain intracellular or sub-cuticular bacteria. The bacteria are autotrophs, as shown by ribulosebisphosphate carboxylase activity of extracts of the bacteria-containing tissues. Comparisons of the 613C values of the bacteria-containing regions and the rest of the tissues indicate substantial transfer of organic carbon, half or more of the nutritional needs of the hosts. The organic carbon is produced by fixation of CO, by the autotrophic bacteria, which oxidize reduced inorganic compounds, notably sulphide, to obtain energy for the process. Similar depletions of 13C were previouslt reported for other autotrophic symbiont-containing bivalves that live in habitats where dissolved sulphide concentrations are 2 or 3 orders of magnitude higher than in the sediments analysed here. This form of nutrition, involving symbiosis with autotrophic bacteria, is evidently not dependent on high levels of dissolved sulphide and appears to be widespread in calcareous reducing sediments of the shelf and continental slope.

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Section: Introductionmentioning

confidence: 99%

13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutricional importance of chemoautotrophic endosymbiotic bacteria

Spiro¹,

Greenwood²,

Southward³

et al. 1986

Mar. Ecol. Prog. Ser.

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“…Chemoautotrophic symbiosis was first described in invertebrates living at the hydrothermal vents but is now known to occur in invertebrates from more accessible habitats, such as shallow-water sediments (4,43). Since their discovery, only one chemosymbiotic animal, the shallow water lucinid Codakia orbicularis (20,22), has been successfully reared to the juvenile stage without symbionts.…”

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confidence: 99%

Respiration Strategies Utilized by the Gill Endosymbiont from the Host Lucinid Codakia orbicularis (Bivalvia: Lucinidae)

Duplessis

Ziebis

Gros

et al. 2004

Appl Environ Microbiol

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The large tropical lucinid clam Codakia orbicularis has a symbiotic relationship with intracellular, sulfide-oxidizing chemoautotrophic bacteria. The respiration strategies utilized by the symbiont were explored using integrative techniques on mechanically purified symbionts and intact clam-symbiont associations along with habitat analysis. Previous work on a related symbiont species found in the host lucinid Lucinoma aequizonata showed that the symbionts obligately used nitrate as an electron acceptor, even under oxygenated conditions. In contrast, the symbionts of C. orbicularis use oxygen as the primary electron acceptor while evidence for nitrate respiration was lacking. Direct measurements obtained by using microelectrodes in purified symbiont suspensions showed that the symbionts consumed oxygen; this intracellular respiration was confirmed by using the redox dye CTC (5-cyano-2,3-ditolyl tetrazolium chloride). In the few intact chemosymbioses tested in previous studies, hydrogen sulfide production was shown to occur when the animal-symbiont association was exposed to anoxia and elemental sulfur stored in the thioautotrophic symbionts was proposed to serve as an electron sink in the absence of oxygen and nitrate. However, this is the first study to show by direct measurements using sulfide microelectrodes in enriched symbiont suspensions that the symbionts are the actual source of sulfide under anoxic conditions

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“…In general, metabolic exchanges between the thioautotrophic symbionts and their hosts have been inferred from enzyme assays (3,44,45), measurements of stable carbon isotope ratios (7,41,44), autoradiography (9,15), or measurements of symbiont respiratory metabolism (2,13,31,32). All these techniques have either no or only very limited potential to study the heterogeneity at the population level.…”

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Characterization of the Population of the Sulfur-Oxidizing Symbiont ofCodakia orbicularis(Bivalvia, Lucinidae) by Single-Cell Analyses

Caro

Gros

Got

et al. 2007

Appl Environ Microbiol

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We investigated the characteristics of the sulfur-oxidizing symbiont hosted in the gills of Codakia orbicularis, a bivalve living in shallow marine tropical environments. Special attention was paid to describing the heterogeneity of the population by using single-cell approaches including flow cytometry (FCM) and different microscopic techniques and by analyzing a cell size fractionation experiment. Up to seven different subpopulations were distinguished by FCM based on nucleic acid content and light side scattering of the cells. The cell size analysis of symbionts showed that the symbiotic population was very heterogeneous in size, i.e., ranging from 0.5 to 5 m in length, with variable amounts of intracellular sulfur. The side-scatter signal analyzed by FCM, which is often taken as a proxy of cell size, was greatly influenced by the sulfur content of the symbionts. FCM revealed an important heterogeneity in the relative nucleic acid content among the subclasses. The larger cells contained exceptionally high levels of nucleic acids, suggesting that these cells contained multiple copies of their genome, i.e., ranging from one copy for the smaller cells to more than four copies for the larger cells. The proportion of respiring symbionts (5-cyano-2,3-ditolyl-terazolium chloride positive) in the bacteriocytes of Codakia revealed that around 80% of the symbionts hosted by Codakia maintain respiratory activity throughout the year. These data allowed us to gain insight into the functioning of the symbionts within the host and to propose some hypotheses on how the growth of the symbionts is controlled by the host.

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Significance of the occurrence of chemoautotrophic bacterial endosymbionts in lucinid clams from Bermuda

Cited by 72 publications

References 23 publications

13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutricional importance of chemoautotrophic endosymbiotic bacteria

13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutricional importance of chemoautotrophic endosymbiotic bacteria

Respiration Strategies Utilized by the Gill Endosymbiont from the Host Lucinid Codakia orbicularis (Bivalvia: Lucinidae)

Characterization of the Population of the Sulfur-Oxidizing Symbiont ofCodakia orbicularis(Bivalvia, Lucinidae) by Single-Cell Analyses

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