Origins of long-chain polyunsaturated fatty acids in the hydrothermal vent worms Ridgea piscesae and Protis hydrothermica

Abstract

Long-chain polyunsaturated fatty acids (PUFAs) are essential nutrients for all marine animals that have previously been studied. Most marine animals obtain long-chain PUFAs from their diets (i.e. as products of photosynthetic processes) and few are known to be able to produce these compounds de novo. Deep-sea vent organisms live in an environment that is relatively isolated from photosynthetic sources of PUFAs, yet some species are known to contain substantial amounts of these compounds. To further understand the origins of PUFAs in deep-sea vent animals, we studied 2 annelid species; a vestimentiferan tubeworm (class Pogonophora) with endosymbiotic bacteria, and a tubicolous serpulid polychaete that feeds heterotrophically. The vestimentiferan tubeworms Ridgeia piscesae from the Juan de Fuca Ridge are rich in the monounsaturated fatty acids 16:1n-7 and 18:1n-7, the polyunsaturated fatty acids (PUFAs) 20:5n-3 and 20:4n-6, and the non-methyleneinterrupted PUFAs 20:2∆5, 13. They also contain small but significant amounts of the PUFAs 18:2n-6, 18:3n-3 and 22:6n-3. δ 13 C values of ca -14 ‰ for 16:1n-7 and 18:1n-7 suggest that these fatty acids are synthesised by chemosynthetic processes at the vent site. A δ 13 C value of -22 ‰ for 20:5n-3 in R. piscesae makes it impossible to conclusively attribute the origin of this fatty acid to either the photic zone or hydrothermal vents. The lipids of the serpulid polychaete Protis hydrothermica from the East Pacific Rise are also rich in 16:1n-7 and contain the unusual PUFAs 18:3n-7. They also contain significant amounts of 20:1n-13 and the PUFAs 20:3n-9, 20:5n-3 and 22:6n-3. Other than 22:6n-3, which had a δ 13 C of -22 ‰, the fatty acids in P. hydrothermica had δ 13 C values ranging from -33 ‰ to -41 ‰. This is consistent with the fatty acids of P. hydrothermica, other than 22:6n-3 but including 20:5n-3, originating from a chemoautotrophic carbon source in the hydrothermal vent. It cannot be excluded that the 22:6n-3 in P. hydrothermica originates in the photic zone. Potential origins of the long-chain PUFAs in hydrothermal vent animals, whether produced by photo-or chemotrophic processes or by pro-or eukaryotic organisms, are considered. KEY WORDS: Hydrothermal vent worms · Nutrition · PUFAs · Stable carbon isotopeResale or republication not permitted without written consent of the publisher

Living on the edge: single-species dominance at the Pakistan oxygen minimum zone boundary

“…nov. was similar to those reported for abyssal polychaetes in the Pacific Ocean (Drazen et al 2008), suggesting a link to the euphotic zone production and ingestion of phytodetritus, as most marine animals cannot synthesize long-chain PUFAs de novo (Pond et al 2002).…”

Fatty acids as dietary tracers in benthic food webs

“…Pond et al (2002) 18:1n-7 indicated a chemosynthetic origin for these FAs, which is consistent with the reliance of R. piscesae on endosymbiotic bacteria . However, δ 13 C values for 20:4n-6 and 20:5n-3 were closer to expected values for photosynthetic microplankton.…”

Abundance and distribution of fatty acids within the walls of an active deep-sea sulfide chimney

“…These PUFAs were reported in previous studies on hydrothermal vent areas, such as sediments (Yamanaka and Sakata, 2004) and Bathymodiolus species (Pranal et al, 1997). Algal-derived PUFAs (20:5ω3 and 22:6ω3) from the photic zone (Sargent et al, 1995) are absent in all present samples, though they were reported previously in the tissue of vent animals, such as shrimps, worms and clams (Pond et al, 1997(Pond et al, , 2002Allen et al, 2001). This is due to algal PUFAs rarely reaching the sulfide chimney due to alteration and/or decomposition during metabolism in the water column (Yamanaka and Sakata, 2004).…”