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Origins of Long-Chain Polyunsaturated Fatty Acids in the Hydrothermal Vent Worms Ridgea Piscesae and Protis Hydrothermica

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Origins of Long-Chain Polyunsaturated Fatty Acids in the Hydrothermal Vent Worms Ridgea Piscesae and Protis Hydrothermica MARINE ECOLOGY PROGRESS SERIES Vol. 225: 219–226, 2002 Published January 11 Mar Ecol Prog Ser Origins of long-chain polyunsaturated fatty acids in the hydrothermal vent worms Ridgea piscesae and Protis hydrothermica David W. Pond1,*, Cathy E. Allen1, Michael V. Bell2, Cindy L. Van Dover 3, Anthony E. Fallick4 , David R. Dixon1, John R. Sargent 2 1Southampton Oceanography Centre, Empress Dock, Southampton SO14 3ZH, United Kingdom 2Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, United Kingdom 3Biology Department, The College of William and Mary, PO Box 8795, 328 Millington Hall, Williamsburg, Virginia 23187, USA 4Scottish Universities Research and Environmental Centre, East Kilbride, Glasgow G75 OQF, United Kingdom 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-methylene- interrupted 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. δ13C 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 δ13C 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 signif- icant 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 δ13C of –22‰, the fatty acids in P. hydrothermica had δ13C 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 isotope Resale or republication not permitted without written consent of the publisher INTRODUCTION 1990). One paradox of the trophic biochemistry of vent invertebrates that remains to be resolved is the source The abundant invertebrate communities endemic to of their long-chain n-3 polyunsaturated fatty acids hydrothermal vent sites in the eastern Pacific are (PUFAs), 20:5n-3 and 22:6n-3. These PUFAs, especially largely nourished by bacterial chemosynthesis (Fisher 20:5n-3, are known to be essential nutrients for all marine animals so far studied, the majority of which *E-mail: [email protected] have been fishes related to aquaculture (Sargent et al. © Inter-Research 2002 · www.int-res.com 220 Mar Ecol Prog Ser 225: 219–226, 2002 1995). Photosynthetic microplankton are the predomi- marker techniques are also useful in understanding nant source of 20:5n-3 and 22:6n-3 in the marine envi- the coupling of vent ecosystems with processes occur- ronment (Sargent et al. 1995), but the distribution of ring in the surface layers of the ocean (Rieley et al. these light-dependent organisms is limited to the 1995, Pond et al. 1997a,c, 2000, Allen et al. 1998). To upper ocean. Long-chain n-3 PUFAs are labile and do investigate the origin(s) of the high levels of 20:5n-3 in not persist in organic matter transferred to the deep Ridgea piscesae, we have employed gas-liquid chro- ocean (Wakeham et al. 1997), so that their supplies to matography coupled with isotope ratio-mass spectrom- deep-sea hydrothermal vents are inevitably limited. etry (GC-IRMS) to determine the δ13C values of indi- Bresiliid shrimp, which dominate the fauna of many vidual fatty acids in adult tubeworms collected from hydrothermal sites along the Mid-Atlantic Ridge (MAR), active vent sites on the Juan de Fuca Ridge. For com- obtain substantial amounts of photosynthetically de- parison, we also analysed the δ13C values of fatty acids rived 20:5n-3 and, especially, 22:6n-3 during their dis- in a species of tubicolous polychaete (Protis hydrother- persive, planktotrophic larval phase (Pond et al. 2000). mica f. Serpulidae) from the East Pacific Rise (EPR). P. Adult shrimp either do not require or are not able to hydrothermica lives in dense colonies on basalt in exploit a source of long-chain n-3 PUFAs at the vent peripheral regions of active vent fields. It is presumed, sites (Pond et al. 2000). Analysis of free-living filamen- by analogy to its shallow-water serpulid relatives, to be tous bacteria attached to bivalve shells and detrital a suspension-feeder with a functional gut. There is no material has provided no evidence of a bacterial source evidence to suggest that this species relies on endo- of 20:5n-3 and 22:6n-3 at MAR vent sites (Pond et al. symbiotic bacteria for its nutrition, although dietary 1998, 2000). roles of episymbiotic and gut bacteria have not been At eastern Pacific vents, vestimentiferan tubeworms eliminated. often dominate the fauna (Fisher 1990, Tunnicliffe et al. 1990). These tubeworms possess a gut only during their early life stages (Jones & Gardiner 1988), and MATERIALS AND METHODS as adults their nutrition is derived from substantial populations of endosymbiotic sulphur-oxidizing bacte- Station locations and description. In 1995, five intact ria (Cavanaugh et al. 1981, Felbeck 1981, Rau 1981, specimens of Ridgeia piscesae were collected from the deBurgh et al. 1989). Ridgeia piscesae, a major compo- High Rise hydrothermal vent field, on the Endeavour nent of the macrobenthos at the Juan de Fuca Ridge segment of the Juan de Fuca Ridge (48° 57.1’ N, in the northeast Pacific (Tunnicliffe & Fontaine 1987, 129° 05.2’ W, approx. 2200 m depth). The worms were Southward et al. 1996), contains substantial amounts of cut immediately below the vestimentum to provide 2 20:5n-3 and also 20:4n-6 (Fullarton et al. 1995, Allen sections of tissue for lipid analysis. The anterior section 1999). The lack of a gut in adult R. piscesae, the comprised the obturaculum and vestimentum that sup- reliance of the tubeworm on endosymbiotic sulphur- ports the branchial plume, and is not known to contain oxidizing bacteria, and its benthic existence deeply bacterial endosymbionts. The posterior section con- removed from photosynthetic sources of long-chain tained the opisthosome, trophosome and gonad tis- n-3 PUFAs make it difficult to reconcile the high levels sues. Three specimens of Protis hydrothermica were of 20:5n-3 in its tissues with a photosynthetic origin. collected from the Genesis site on the EPR during the Furthermore, vestimeniferans produce lecithotrophic ‘HOPE 1999’ cruise (12° 48.7 N, 103° 56.4 W, Dive 1383, larvae (Tyler & Young 1999) and their post-larvae 2600 m: Lallier et al. 1999). The calcareous tubes of the settle at suitable vent sites when very small (South- polychaetes were attached to basalt located within 1 m ward 1988). It seems improbable, therefore, that their of the base of the vent discharge. Intact polychaetes larvae could accumulate substantial reserves of photo- were removed from their tubes and dissected into synthetically-derived material. This contrasts with the crown (including thorax) and abdominal sections. All bresiliid shrimp found at Mid-Atlantic Ridge vents tissues were frozen (–70°C) immediately on board ship which, as noted above, accumulate relatively high and transported in dry ice to the UK, where they were levels of photosynthetically-derived long-chain n-3 stored at –70°C until analysis. PUFAs during larval and early juvenile development Lipid analyses. Total lipid was extracted from the tis- (Pond et al. 1997a,b,c, 2000, Allen et al. 1998). sues using chloroform:methanol (2:1 vol:vol) (Folch et Characterization of δ13C values of lipid biomarkers in al. 1957). Aliquots of total lipid were transesterified in hydrothermal vent organisms is a valuable technique methanol containing 1.5% sulphuric acid at 50°C for for studying nutritional relationships between the ani- 16 h to generate fatty acid methyl esters (FAMEs; mal and bacterial communities that exploit vent envi- Christie 1982). FAME were purified by thin-layer chro- ronments and cold-seep environments (Abrajano et al. matography using a hexane:diethyl ether:acetic acid 1994, Jahnke et al. 1995, Pond et al. 1998). Lipid bio- (90:10:1, vol:vol:vol) solvent system. Purified FAMEs Pond et al.: Polyunsaturated fatty acids in hydrothermal vent worms 221 were dissolved in hexane to a concentration of 2 mg as δ13C and relative to that of Peedee Belemnite (‰ ml–1 and analyzed by gas chromatography on a 6000 v-PDB). Replicate injections indicate that analytical Vega series (Carlo Erba, Milan, Italy) fitted with a BP20 precision was ± 0.4‰ or better.
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