Alissa J. Arp

Metabolic and Blood Gas Transport Characteristics of the Hydrothermal Vent Bivalve Calyptogena magnifica

Individual Calyptogena magnifica are able to regulate their oxygen consumption rates down to low partial pressures of oxygen. Their rates of oxygen consumption are comparable to those of active shallow-living bivalves at comparable temperatures. Rates of carbon dioxide production relative to oxygen consumption in the absence of sulfide indicate a predominately heterotrophic metabolism. Calyptogena magnifica individuals do not show significant uptake of methane so this is unlikely to be an important external metabolite for these clams. Sulfide levels in the blood and gills of freshly recovered clams were high (up to 1.9 mM) and were generally in excess of estimated environmental sulfide levels (<0.2 mM). Sulfur-metabolizing ability (measured as ATP sulfurylase activity) of the gill tissue including endosymbiotic bacteria was substantial and variable, suggesting microhabitat variation. Blood serum separated from erythrocytic Hb showed marked sulfide accumulation and may function for sulfide transport as well as to protect the sulfide-sensitive hemoglobin by binding free sulfide. The hypothesis that C. magnifica may take up sulfide through the foot (which is extended into the vent water in the rock fissures) and transport it to the bacteria in the gills via the sulfide-binding component in the blood serum while simultaneously taking up oxygen and carbon dioxide through the siphon (which is extended upward into the ambient bottom water) is explored.

Sulfide permeability in the marine invertebrate Urechis caupo

SummaryHydrogen sulfide can reach toxic concentrations in the burrow-water of the echiuran worm Urechis caupo during low tide. Its two large epithelial surfaces, the thick muscular body wall and the thin-walled hindgut are in constant contact with the environment. Hindgut inflation of up to 2 ml water·g wet weight-1 causes tissue stretch. To determine if these body surfaces present a barrier to sulfide influx, the total permeability coefficient PT was measured at different degrees of stretch in diffusion chambers at pH 6.0, 7.0, and 8.0, and specific permeability coefficients PH2S and PHS- were calculated. Both the body wall and the hindgut were more permeable to H2S than HS-. The body wall showed no significant increase in sulfide permeability with natural degrees of stretch, and the mean PH2S and PHS- were 0.17 and 0.063 cm·h-1, respectively. The sulfide permeability of the hindgut was increased by stretch, with the relative permeability of H2S increasing faster than that of HS-. Unstretched hindgut mean PH2S and PHS- were 0.095 and 0.11 cm·h-1, respectively, and stretched hindgut mean PH2S and PHS- were 1.8 and 0.16 cm·h-1, respectively. A model of sulfide influx in the natural environment indicates that even if the hindgut is kept uninflated, the coelomic fluid of U. caupo would have toxic sulfide concentrations well before the end of a 2-h tidal exposure in the absence of a sulfide elimination mechanism.

Oxygenation properties of the two co-occurring hemoglobins of the tube worm Riftia pachyptila

Riftia pachyptila vascular blood and coelomic fluid contain two hemoglobin molecules that differ in their distribution and physical properties. The present study of the two isolated hemoglobins shows that both have an extremely high affinity for oxygen, but differ in their oxygenation characteristics. FI, the larger molecular weight (Mr) fraction (1,700,000), has a lower oxygen affinity, a well defined pH Bohr effect, and high cooperativity of oxygen binding. FII, the lower Mr fraction (400,000) has a higher oxygen affinity, no pH Bohr effect, and reduced cooperativity of oxygen binding. Both hemoglobins show marked effects of temperature on oxygen binding, and no effect of heme concentration or the presence of sulfide on oxygen affinity. The differences in the oxygenation properties and distribution of the two hemoglobins in the body fluids of Riftia pachyptila may allow them to play different roles in oxygen transport and storage for the animal which lives in the variable environment of the hydrothermal vents.

The effects of sulfide on the anaerobic metabolism of two congeneric species of mudflat clams

Abstract 1. 1. Mudflat dwelling bivalves undergo intermittent periods of anoxia and elevated sulfide during tidal exposure. 2. 2. The sulfide uptake, tolerance and changes in anaerobic metabolite concentrations during sulfide exposure were investigated in two congeneric clam species Macoma secta and M. nasuta . 3. 3. Both species showed a lower tolerance to anoxia in the presence of sulfide. 4. 4. Both species had the ability to maintain an internal sulfide concentration below that of the environment. 5. 5. Anaerobiosis in the presence of sulfide did not affect the utilization of glucose, glycogen, and aspartate energy reserves in M. secta while M. nasuta showed a significantly higher overall glycogen reserve, and a lower utilization of glucose and aspartate. 6. 6. Octopine levels in both clams were elevated following anoxic incubation in the presence of sulfide. 7. 7. The results suggest that M. nasuta s higher sulfide tolerance may be due to regulation of basal metabolic rate during anoxic sulfide exposure.

Morphological adaptations of the respiratory hindgut of a marine echiuran worm

The echiuran worm Urechis caupo lives in U‐shaped burrows in marine mudflats where levels of toxic hydrogen sulfide increase and water becomes hypoxic during low tide. Even in this low oxygen and high sulfide environment, the animal is capable of maintaining aerobic respiration. Gas exchange occures across both the body wall and hindgut. The hindgut functions as a type of water lung and is a thin walled, highly convoluted structure capable of considerable dilatation. It is rhythmically ventilated with water and its role as a respiratory organ becomes increasingly important as ambient pO2 drops. In the deflated hindgut light microscopy reveals a pseudostratified appearing innermost mucosal epithelium composed of columnar cells with nuclei at different levels. When the hindgut is fully inflated, ultrastructural studies show a simple columnar epithelium with the nuclei at the same level. Ultrastructurally, the free surface of the hindgut cells bears numerous microvilli and a few cilia. The lateral cell membranes are highly folded in the deflated hindgut, but these folds are not visible in the fully inflated hindgut. The cytoplasm contains osmiophilic bodies which show a partially lamellated pattern which may be sulfide oxidizing bodies involved in sulfide detoxification. In the fully inflated hindgut, the entire perimeter of the lumenal mucosa is covered by electron dense inclusions, whose exact fuction is unknown. The lack of structural information on the respiratory organ of this echiuran worm renders the interpretation of its morphological and histological features at the ultrastructural level difficult, although the present study has broadened our understanding of the structural adaptations of the hindgut as a respiratory organ.

Aerobic Respiration during Sulfide Exposure in the Marine Echiuran Worm Urechis caupo

Urechis caupo inhabit U-shaped burrows in mudflats where they are exposed to toxic hydrogen sulfide. During tidal exposure sulfide levels average 27μM and oxygen levels average 77 mmHg. The oxygen consumption rate (V̇o2) of U. caupo was measured at varying partial pressures of oxygen and with and without sulfide to investigate whether aerobic respiration is maintained during tidal exposure. Animals exposed to PO₂s as low as 32 mmHg and sulfide concentrations of less than 30 μM did not significantly change V̇o2 (mean V̇o2 = 0.039 ± 0.016 mL O₂·g⁻¹·h⁻¹), although there was a general trend of increased V̇o2 with increased sulfide. We investigated whether this animal avoids sulfide toxicity by oxidation of sulfide catalyzed by coelomic fluid hematin. A positive correlation was found between V̇o2 and hematin concentration for animals exposed to 4-29 μM sulfide. The V̇o2 of coelomic fluid samples measured in vitro showed a peak V̇o2 and positive correlation with hematin concentration at 17 μM sulfide. Oxygen consumption rates of hematin isolated from the coelomic fluid showed a positive correlation between V̇o2 and sulfide concentration at 1.0 and 1.8 mM hematin, and V̇o2 was significantly greater at 1.8 mM hematin in the presence of sulfide. These results suggest that oxygen consumption in U. caupo is not inhibited at environmental oxygen and sulfide levels and that the elevation in V̇o2 observed in the presence of sulfide in vitro may be due to oxidation of sulfide by coelomic fluid hematin.

Thiosulfate elimination and permeability in a sulfide-adapted marine invertebrate.

Oxidation of hydrogen sulfide to thiosulfate is one of the best‐characterized mechanisms by which animals adapted to sulfide minimize its toxicity, but the mechanism of thiosulfate elimination in these animals has remained unclear. In this study, we examined the accumulation and elimination of thiosulfate in the sulfide‐adapted marine worm Urechis caupo. The coelomic fluid of U. caupo exposed to 50–100 μmol L−1 sulfide in hypoxic seawater (Po2 ca. 10 kPa) accumulated ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape

Water lung and body wall contributions to respiration in an echiuran worm.

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