Sulfide and Carbon Dioxide Uptake by the Hydrothermal Vent Clam,<i>Calyptogena magnifica,</i>and Its Chemoautotrophic Symbionts

Childress, James J.; Fisher, Charles R.; Favuzzi, J.A.; Sanders, N. K.

doi:10.1086/physzool.64.6.30158224

Cited by 71 publications

(46 citation statements)

References 28 publications

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“…They thus strengthen the view that the relationship between bacteria and shrimp is mutualistic: the epibionts supply carbon compounds to the shrimp and the shrimp, thanks to its gill chamber flow and its swimming behaviour, offers them protection and a supply of chemical compounds, maintaining their position at the oxic/anoxic interface around active chimneys Segonzac et al, 1993). The R. exoculata bacterial epibiosis can thus be regarded as a true mutualistic trophic ectosymbiosis, similar to what is known about the chemosynthetic endosymbiosis of organisms such as R. pachyptila (Felbeck, 1981;Fisher et al, 1989), Calyptogena magnifica (Childress et al, 1991) and S. velum (Stewart and Cavanaugh, 2006;Scott and Cavanaugh, 2007). Finally, the view that bacterial products are assimilated across the shrimp integument rather than via the DT is strongly supported by: (1) the significant incorporation of both 14 C-acetate and 3 Hlysine after an incubation time as short as 1 h. This is insufficient for uptake by ingestion assimilation, which commonly takes several hours (ingestion assimilation of carbon from bicarbonate, for example, requires prior incorporation by the bacteria, followed by grazing of bacteria from the MP) (Chipps, 1998;Hoyt et al, 2000); (2) the high incorporation levels recorded in the gill chamber integument lining (OB, Gi), as opposed to (3) the much lower levels recorded in the DT (Figure 6).…”

Section: Bacteria-host Transfersmentioning

confidence: 73%

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

et al. 2012

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The shrimp Rimicaris exoculata dominates several hydrothermal vent ecosystems of the MidAtlantic Ridge and is thought to be a primary consumer harbouring a chemoautotrophic bacterial community in its gill chamber. The aim of the present study was to test current hypotheses concerning the epibiont's chemoautotrophy, and the mutualistic character of this association. Invivo experiments were carried out in a pressurised aquarium with isotope-labelled inorganic carbon (NaH 13 CO 3 and NaH 14 CO 3 ) in the presence of two different electron donors (Na 2 S 2 O 3 and Fe 2 þ ) and with radiolabelled organic compounds ( 14 C-acetate and 3 H-lysine) chosen as potential bacterial substrates and/or metabolic by-products in experiments mimicking transfer of small biomolecules from epibionts to host. The bacterial epibionts were found to assimilate inorganic carbon by chemoautotrophy, but many of them (thick filaments of epsilonproteobacteria) appeared versatile and able to switch between electron donors, including organic compounds (heterotrophic acetate and lysine uptake). At least some of them (thin filamentous gammaproteobacteria) also seem capable of internal energy storage that could supply chemosynthetic metabolism for hours under conditions of electron donor deprivation. As direct nutritional transfer from bacteria to host was detected, the association appears as true mutualism. Import of soluble bacterial products occurs by permeation across the gill chamber integument, rather than via the digestive tract. This first demonstration of such capabilities in a decapod crustacean supports the previously discarded hypothesis of transtegumental absorption of dissolved organic matter or carbon as a common nutritional pathway.

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Section: Bacteria-host Transfersmentioning

confidence: 73%

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

et al. 2012

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“…Lamellibrachia values from Freytag et al (2001). Calyptogena rates are based on 14 C fixation by gill pieces (Childress et al, 1991b). Bathymodiolus brevior and Ifremeria nautilei rates from Henry et al (2008).…”

Section: Comparing Physiological and Morphological Attributes Of Chemmentioning

confidence: 99%

“…This is further emphasized by the relatively large diffusion distances from water to blood observed in some of these symbioses. For example the vesicomyid Calyptogena elongata has a diffusion distance of about 6m (Childress et al, 1991b) while Bathymodilus childressi and B. thermophilus have diffusion distances of about 12 and 17m, respectively (Fisher et al, 1987), which reduce their effectiveness in passing gases to and from the hemolymph. Thus, their critical importance is as a very expanded surface, which is continuously and effectively exposed to the highest concentrations of the required metabolites that are available in their environments.…”

Section: Characteristics and Functioning Of Mollusc Chemoautotrophic mentioning

confidence: 99%

The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities

Childress

Girguis

2011

Journal of Experimental Biology

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SummaryWhile chemoautotrophic endosymbioses of hydrothermal vents and other reducing environments have been well studied, little attention has been paid to the magnitude of the metabolic demands placed upon the host by symbiont metabolism and the adaptations necessary to meet such demands. Here we make the first attempt at such an evaluation, and show that moderate to high rates of chemoautotrophic or methanotrophic metabolism impose oxygen uptake and proton equivalent elimination demands upon the hosts that are much higher than is typical for the non-symbiotic annelid, bivalve and gastropod lineages to which they are related. The properties of the hosts are described and compared to determine which properties are associated with and predictive of the highest rates. We suggest that the high oxygen demand of these symbionts is perhaps the most limiting flux for the symbioses. Among the consequences of such demands has been the widespread presence of circulating and/or tissue hemoglobins in these symbioses that are necessary to support high metabolic rates in thioautotrophic endosymbioses. We also compare photoautotrophic with chemoautotrophic and methanotrophic endosymbioses to evaluate the differences and similarities in physiologies. These analyses suggest that the high demand for oxygen by chemoautotrophic and methanotrophic symbionts is likely a major factor precluding their endosymbiosis with cnidarians. Supplementary material available online at

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“…Members of this group are closely related to thiotrophic bacteria that obtain energy from the oxidation of reduced sulfur compounds (Distel et al, 1988). Similar to other symbiotic relationships in sulfide-rich marine ecosystems, the host provides access to reduced sulfur sources for autotrophic bacteria and the bacterial symbionts provide the host with a source of organic carbon (Childress et al, 1991;Robinson and Cavanaugh, 1995).…”

Section: Introductionmentioning

confidence: 99%

Sulfur oxidizers dominate carbon fixation at a biogeochemical hot spot in the dark ocean

et al. 2013

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Bacteria and archaea in the dark ocean (4200 m) comprise 0.3-1.3 billion tons of actively cycled marine carbon. Many of these microorganisms have the genetic potential to fix inorganic carbon (autotrophs) or assimilate single-carbon compounds (methylotrophs). We identified the functions of autotrophic and methylotrophic microorganisms in a vent plume at Axial Seamount, where hydrothermal activity provides a biogeochemical hot spot for carbon fixation in the dark ocean. Free-living members of the SUP05/Arctic96BD-19 clade of marine gamma-proteobacterial sulfur oxidizers (GSOs) are distributed throughout the northeastern Pacific Ocean and dominated hydrothermal plume waters at Axial Seamount. Marine GSOs expressed proteins for sulfur oxidation (adenosine phosphosulfate reductase, sox (sulfur oxidizing system), dissimilatory sulfite reductase and ATP sulfurylase), carbon fixation (ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO)), aerobic respiration (cytochrome c oxidase) and nitrogen regulation (PII). Methylotrophs and iron oxidizers were also active in plume waters and expressed key proteins for methane oxidation and inorganic carbon fixation (particulate methane monooxygenase/methanol dehydrogenase and RuBisCO, respectively). Proteomic data suggest that free-living sulfur oxidizers and methylotrophs are among the dominant primary producers in vent plume waters in the northeastern Pacific Ocean.

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Sulfide and Carbon Dioxide Uptake by the Hydrothermal Vent Clam,Calyptogena magnifica,and Its Chemoautotrophic Symbionts

Cited by 71 publications

References 28 publications

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities

Sulfur oxidizers dominate carbon fixation at a biogeochemical hot spot in the dark ocean

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