Functional anatomy of the respiratory system of Branchipolynoe species (Polychaeta, Polynoidae), commensal with Bathymodiolus species (Bivalvia, Mytilidae) from deep-sea hydrothermal vents

Abstract

The gills of three species of Branchipolynoe have been studied in order to better understand the morphological and anatomical adaptations of their respiratory system. These Polynoidae live commensally inside the pallial cavity of different species of Bathymodiolus (Mytilidae), found clustered near deep-sea hydrothermal vents and cold seeps, and which harbor chemolithoautotrophic bacteria in their gills. As the mussels exploit hydrothermal fluid, the pallial cavity is perfused with a sulfide-rich hydrothermal water. The gills of Branchipolynoe species are well-developed branched outgrows of the body wall, located on the parapodia, and filled with coelomic fluid. They do not contain blood vessels. Living animals are red, due to the presence of extracellular hemoglobins in the coelom. The gill epidermis is made of supporting cells and a few ciliated cells arranged in longitudinal rows along the branches. Myoepithelial and ciliated cells line the interior of the coelomic cavity which contains the respiratory pigments. Coelomic fluid circulation inside the gills and body cavity is probably facilitated by both the cilia and myoepithelial contractions. The cuticle, the epidermis, and the coelomic epithelium are completely devoid of bacteria. The gill surface areas per unit body weight and the minimum diffusion distances, between external milieu and coelomic hemoglobins, have been calculated and compared with data already obtained on vascular gills of littoral or hydrothermal species of Polychaeta. In Branchipolynoe species, the respiratory surface area is very large, similar to that of a free-living hydrothermal species Alvinella pompejana, and the minimum diffusion distance is short, similar to that of the littoral species Arenicola marina. Although the organization of these coelomic gills in Branchipolynoe species is totally different from that of usual vascular gills, their characteristics represent a unique and effective respiratory system in Polynoidae which has adapted to the hypoxic and sulfiderich micro-habitat which probably holds in the mantle cavity of vent mussels. In the gill epidermis, numerous secondary and large compound lysosomes are present which might be involved in sulfide detoxification.& b d y :

Molecular and functional adaptations in deep-sea hemoglobins

“…The cooperativity coefficient of the two Hbs does not exceed 1.9, and is usually close to unity [74]. Furthermore, the Hb-containing coelomic fluid does not perfuse the gills unidirectionally [75] suggesting that the Hbs do not play a major role in O 2 transport and probably form an O 2 store. The weight-specific heme content varies inversely with size ( Fig.…”

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

“…Regardless of the mechanism, mitochondria are likely to be particularly susceptible to damage from sulfide exposure. This prompted Arp et al (1995) to hypothesize that at least some EDOs (which in that paper were termed SOBs) of sulfide‐exposed annelids are “secondary lysosomes” containing sulfide‐damaged mitochondria that have been phagocytosed and are in various stages of degradation (Arp et al 1995, also see Hourdez & Jouin‐Toulmond 1998; Hourdez et al 2001).…”

Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates

“…However, their gills are mere finger-like extension of their body-wall that are perfused by the coelomic fluid and not by blood vessels. The bodywall is very Jouin and Gaill (1990); b Andersen et al (2002); c Hourdez and JouinToulmond (1998); d Jouin-Toulmond and Hourdez (2006); e Jouin and Toulmond (1989); f Hourdez et al (2001) thin there (typically 10 lm) whereas it is 150 lm thick anywhere else on the body (Hourdez and Jouin-Toulmond 1998).…”