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Marine free-living nematodes associated with symbiotic bacteria in deep-sea canyons of north-east Atlantic Ocean

Published online by Cambridge University Press:  06 February 2012

Alexei V. Tchesunov ,
Jeroen Ingels  and
Ekaterina V. Popova
Alexei V. Tchesunov*
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, Lomonosov's Moscow State University, Moscow, 119991, Russia
Jeroen Ingels
Affiliation:
Marine Biology Department, Gent University, Krijgslaan 281 S8, 9000 Ghent, Belgium
Ekaterina V. Popova
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, Lomonosov's Moscow State University, Moscow, 119991, Russia
*
Correspondence should be addressed to: A.V. Tchesunov, Department of Invertebrate Zoology, Faculty of Biology, Lomonosov's Moscow State University, Moscow, 119991, Russia email: [email protected]
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Abstract

Two nematode species living in association with chemoautotrophic prokaryotes were found in two deep-sea canyon/channel systems, the Whittard Canyon and Gollum Channels, north-east Atlantic. Parabostrichus bathyalis gen. nov. sp. nov. (Desmodorida: Desmodoridae: Stilbonematinae) relates to Eubostrichus Greeff 1869 but differs in having well-developed paired dorso-caudal apophyses of the gubernaculum, small pre- and postcloacal latero-ventral papillae with short apical setae, elongate tail with slender posterior portion, and the absence of thorn-like setae (porids) in males. Body of P. bathyalis is loosely covered with elongate cells of prokaryote ectosymbionts. Astomonema southwardorum Austen et al. 1993, originally found at a methane seep pockmark in the North Sea, constitutes a significant portion of nematode communities in certain areas of the deep-sea canyon/channel systems. Taxonomic difficulties within Astomonematinae are discussed in light of the character state of paired male gonads discovered in A. southwardorum. Canyon populations of A. southwardorum are characterized by frequent loss of part of the hind body and wound healing posterior to the vulva in females. Both species tend to occur in deeper subsurface layers of the bottom sediment. Abundance of the nematode species associated with aggregations of ectosymbiotic (Parabostrichus) and endosymbiotic (Astomonema) chemoautotrophic bacteria may indicate reduced conditions at sites in these deep-sea canyons/channels and suggests a potentially substantial ecological role for chemolitotrophic fauna there.

Keywords

Astomonemabathyalchemoautotrophydescriptionfree-living nematodesnew speciesParabostrichusStilbonematinaesymbiotic bacteriataxonomy
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 6 , September 2012 , pp. 1257 - 1271
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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References

REFERENCES

Austen, M.C., Warwick, R.M. and Ryan, K.P. (1993) Astomonema southwardorum sp. nov., a gutless nematode dominant in a methane seep area in the North Sea. Journal of the Marine Biological Association of the United Kingdom 73, 627–634.CrossRefGoogle Scholar
Bayer, Ch., Heindl, N.L., Rinke, Ch., Lücker, S., Ott, J.A. and Bulgheresi, S. (2009) Molecular characterization of the symbionts associated with marine nematodes of the genus Robbea. Environmental Microbiology Reports 1, 136–144.Google Scholar
Bernhard, J.M., Buck, K.R., Farmer, M.A. and Bowser, S.S. (2000) The Santa Barbara Basin is a symbiosis oasis. Nature 403, 77–80.Google Scholar
Bird, A.F. and Bird, J. (1991) The structure of nematodes. 2nd edition. San Diego, CA: Academic Press.Google Scholar
Bongers, T. (1983) Bionomics and reproductive cycle of the nematode Leptosomatum bacillatum living in the sponge Halichondria panacea. Netherlands Journal of Sea Research 17, 39–46.CrossRefGoogle Scholar
Cobb, N.A. (1925) Proceedings of the seventy-ninth to eighty-second meeting of the Helminthological Society of Washington. Journal of Parasitology 2, 222.Google Scholar
De Leo, F.C., Smith, C.R., Rowden, A.A., Bowden, D.A. and Clark, M.R. (2010) Submarine canyons: hotspots of benthic biomass and productivity in the deep sea. Proceedings of the Royal Society B: Biological Sciences. Doi: 10.1098/rspb.2010.0462.Google Scholar
Gerlach, S.A. (1963) Freilebende Meeresnematoden von den Malediven II. Kieler Meeresforschungen 18, 67–103.Google Scholar
Giere, O. (2009) Meiobenthology, the microscopic motile fauna of aquatic sediments. Berlin and Heidelberg: Springer-Verlag.Google Scholar
Giere, O., Windoffer, R. and Southward, E.C. (1995) The bacterial endosymbiosis of the gutless nematode, Astomonema sothwardorum: ultrastructural aspects. Journal of the Marine Biological Association of the United Kingdom 75, 153–164.CrossRefGoogle Scholar
Harris, P.T. and Whiteway, T. (2011) Global distribution of large submarine canyons: geomorphic differences between active and passive continental margins. Marine Geology 285, 69–86.CrossRefGoogle Scholar
Heip, C., Vincx, M. and Vranken, G. (1985) The ecology of marine nematodes. Oceanography and Marine Biology: an Annual Review 23, 399–489.Google Scholar
Hendelberg, M. (1977) Paralinhomoeus gerlachi (Linhomoeidae), a new marine nematode from Bermuda. Zoon 5, 79–86.Google Scholar
Hentschel, U., Berger, E.C., Bright, M., Felbeck, H. and Ott, J.A. (1999) Metabolism of nitrogen and sulfur in ectosymbiotic bacteria of marine nematodes (Nematoda, Stilbonematinae). Marine Ecology Progress Series 183, 149–158.CrossRefGoogle Scholar
Hopper, B.E. and Cefalu, R.C. (1973) Free-living marine nematodes from Biscayne Bay, Florida V. Stilbonematinae: contributions to the taxonomy and morphology of the genus Eubostrichus Greef and related genera. Transactions of the American Microscopical Society 92, 578–591.Google Scholar
Ingels, J., Billett, D.S.M., Wolff, G., Kiriakoulakis, K. and Vanreusel, A (2011b) Structural and functional diversity of Nematoda in relation with environmental variables in the Setúbal and Cascais canyons, Western Iberian Margin. Deep-Sea Research Part II: Topical Studies in Oceanography 58, 2354–2368.CrossRefGoogle Scholar
Ingels, J., Kiriakoulakis, K., Wolff, G.A. and Vanreusel, A. (2009) Nematode diversity and its relation to quantity and quality of sedimentary organic matter in the Nazaré Canyon, Western Iberian Margin. Deep-Sea Research Part I: Oceanographic Research Papers 56, 1521–1539.Google Scholar
Ingels, J., Tchesunov, A. and Vanreusel, A. (2011a) Meiofauna in the Gollum Channels and the Whittard Canyon, Celtic Margin: how local environmental conditions shape nematode structure and function. PLoS ONE 6, e20094. doi:10.1371/journal.pone.0020094.CrossRefGoogle ScholarPubMed
Ingels, J., Van Rooij, D. and Vanreusel, A. (2006) HERMES RV Belgica 2006/13 Biology cruise report (23–29 June 2006): Gollum Channels and Whittard Canyon.Google Scholar
Kito, K. (1989) A new mouthless marine nematode from Fiji. Journal of Natural History 23, 635–642.CrossRefGoogle Scholar
Kito, K. and Aryuthaka, Ch. (2006) New mouthless nematode of the genus Parastomonema Kito, 1989 (Nematoda: Siphonolaimidae) from a mangrove forest on the coast of Thailand, and erection of the new subfamily Astomonematinae within the Siphonolaimidae. Zootaxa 1177, 39–49.CrossRefGoogle Scholar
Korotkova, G.P. and Agafonova, L.A. (1976) Experimental morphological study of reparative abilities of the nematode Pontonema vulgare. Archives of Anatomy, Histology and Embryology 70, 90–98. [In Russian, with English summary.]Google Scholar
Lampitt, R.S., Raine, R.C.T., Billett, D.S.M. and Rice, A.L. (1995) Material supply to the European continental slope: a budget based on benthic oxygen demand and organic supply. Deep-Sea Research Part I: Oceanographic Research Papers 42, 1865–1873.CrossRefGoogle Scholar
Longhurst, A., Sathyendranath, S., Platt, T. and Caverhill, C. (1995) An estimate of global primary production in the ocean from satellite radiometer data. Journal of Plankton Research 17, 1245–1271.Google Scholar
McClain, C.R. and Barry, J.P. (2010) Habitat heterogeneity, disturbance, and productivity work in concert to regulate biodiversity in deep submarine canyons. Ecology 91, 964–976.Google Scholar
Mokievsky, V.O., Udalov, A.A. and Azovskii, A.I. (2007) Quantitative distribution of meiobenthos in deep-water zones of the World Ocean. Oceanology 47, 797–813.Google Scholar
Musat, N., Giere, O., Gieseke, A., Thiermann, F., Amann, R. and Dubilier, N. (2007) Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp. from the Bahamas. Environmental Microbiology 9, 1345–1353.Google Scholar
Ott, J.A. (1972) Twelve new species of nematodes from an intertidal sandflat in North Carolina. Internationale Revue der gesamten Hydrobiologie und Hydrographie 57, 463–496.Google Scholar
Ott, J.A. and Novak, R. (1989) Living at an interface: meiofauna at the oxygen/sulfide boundary of marine sediments. In Ryland, J.S. and Tyler, P.A. (eds) Reproduction, genetics and distribution of marine organisms. Fredensborg, Denmark: Olsen & Olsen, pp. 415–422.Google Scholar
Ott, J., Bright, M. and Bulgheresi, S. (2004a) Marine microbial thiotrophic ectosymbioses. Oceanography and Marine Biology: an Annual Review 42, 95–118.Google Scholar
Ott, J., Bright, M. and Bulgheresi, S. (2004b) Symbioses between marine nematodes and sulphur-oxidizing chemoautotrophic bacteria. Symbiosis 36, 102–126.Google Scholar
Ott, J.A., Novak, R., Schiemer, P., Hentschel, U., Nebelsick, M. and Polz, M. (1991) Tackling the sulphide gradient: a novel strategy involving marine and chemoautotrophic ectosymbionts. P.S.Z.N. I.: Marine Ecology 12, 261–279.Google Scholar
Ott, J.A., Rieger, G. and Enderes, F. (1982) New mouthless interstitial worms from the sulphide system: symbiosis with prokaryotes. P.S.Z.N.I.: Marine Ecology 3, 313–333.Google Scholar
Riemann, F., Thiermann, F. and Bock, L. (2003) Leptonemella species (Desmodoridae, Stilbonematinae), benthic marine nematodes with ectosymbiotic bacteria from littoral sand of the North Sea island of Sylt: taxonomy and ecological aspects. Helgoland Marine Research 57, 118–131.CrossRefGoogle Scholar
Schiemer, F., Novak, R. and Ott, J. (1990) Metabolic studies on thiobiotic free-living nematodes and their symbiotic microorganisms. Marine Biology 106, 129–137.Google Scholar
Soltwedel, T. (2000) Metazoan meiobenthos along continental margins: a review. Progress in Oceanography 46, 59–84.CrossRefGoogle Scholar
Tchesunov, A.V. (1986) Two new sympatric species of nematodes from the genus Megadesmolaimus (Monhysterida, Linhomoeidae) in the Red Sea. Zoologichesky Zhurnal 65, 819–828. [In Russian, with English summary.]Google Scholar
Van Gaever, S., Moodley, L., de Beer, D. and Vanreusel, A. (2006) Meiobenthos at the Arctic Håkon Mosby Mud Volcano, with a parental-caring nematode thriving in sulphide-rich sediments. Marine Ecology Progress Series 321, 143–155.Google Scholar
Vincx, M. (1996) Meiofauna in marine and fresh water sediments. In Hall, G.S. (ed.) Methods for the examination of organismal diversity in silts and sediments. Cambridge: CAB International and Cambridge University Press, pp. 214–248.Google Scholar
Vitiello, P. (1970) Nématodes libres marins des vases profondes du Golfe du Lion. Téthys 2, 647–690.Google Scholar