Epidermal ultrastructure and implications for sulfide tolerance in six species of deep‐sea polychaetes

Abstract

Ultrastructural characteristics of the epidermis of 5 deep-sea vestimentiferan tube worms and an orbiniid worm were similar to those described from other organisms inhabiting sulfidic environments. The integument was composed of a simple or pseudostratified layer of columnar or cuboidal cells, covered by a cuticle of varying thickness, and rested on an extracellular matrix. Unusual mitochondria1 morphology was observed in the peripheral region of the epidermis, characterized by an electron-dense matrix and granules. The abnormal size, shape, and reduced array of cristae in these mitochondria may have resulted from environmental stress. Mitochondria in the inner epidermal layers, where they are more protected from sulfide exposure, displayed normal morphology. The seep vestimentiferans (Seepiophila jonesi and Lamellibrachia cf. luymesi) exhibited numerous electron-dense organelles, similar in morphology to cytolysosomes and previously described as sulfide oxidizing bodies, while in the 3 vent vestimentiferans (Riftia pachyptila, Tevnia jerichonana, and Oasisia alvinae) and the seep orbiniid Methanoaricia dendrobranchiatu, fewer of these organelles were observed. Energy dispersive x-ray microanalysis of these electron-dense organelles indicated the presence of sulfur, iron, zinc, and copper, as well as lesser amounts of other elements. We propose that these epidermal cytolysosomes are morphologically similar to previously described sulfide oxidizing bodies that have been hypothesized to play a role in maintaining aerobically poised animal metabolism in sulfide-enriched habitats.

Hypotaurine and thiotaurine as indicators of sulfide exposure in bivalves and vestimentiferans from hydrothermal vents and cold seeps

“…1996), and other mechanisms of intracellular defense against sulfide have been proposed. For example, there are specialized sulfide‐oxidizing organelles in epidermal tissue in some polychaetes including vestimentiferans (Menon et al. 2003).…”

Thiotaurine and hypotaurine contents in hydrothermal‐vent polychaetes without thiotrophic endosymbionts: correlation With sulfide exposure

“…These include the following: sulfide-binding proteins (e.g., modified hemoglobins) in body fluids of endosymbiont-bearing animals, for transporting sulfide nontoxically (e.g., Arp et al,'87;Childress et al,'93;Kraus,'95); external tubes and mucus of some polychaetes, which may reduce diffusion of sulfide into the animal; microbes living on the tubes, which oxidize sulfide before it can enter the animal (Juniper and Martineu,'95); specialized sulfide-oxidizing organelles in epidermal tissue in some polychaetes from sulfide-rich habitats (Arp et al, '95;Menon et al, 2003); conversion to thiosulfate or elemental sulfur (Vetter, '85;Powell and Somero, '86;Arp et al, '95;Arndt et al, 2001); and binding to intracellular metals, protein, and glutathione (Vismann,'91). Among vent animals without endosymbionts, P. palmiformis has been reported to have high (but variable) sulfide levels in the blood along with a sulfide-binding hemoglobin-like protein (Martineu et al,'97).…”

Rapid induction and disappearance of electron‐dense organelles following sulfide exposure in the marine annelid Branchioasychis americana

“…The EDO quantity in the body wall of B. americana was ∼10‐fold higher than in the body wall or hindgut in U. caupo , but it increased by approximately the same proportion as the hindgut in U. caupo when individuals of B. americana were exposed to sulfide (although note that the exposure duration was one‐third as long in the present study). Even so, the EDO quantity in B. americana after sulfide exposure is still far less than in cells from some hydrocarbon seep and hydrothermal vent annelids, in which the majority of the non‐nuclear cell volume may be comprised of such organelles (Menon et al 2003). EDO quantity was variable at each sampling time, especially at 24‐h sulfide exposure, but it is unknown whether this is primarily due to variation between or within animals.…”