Marine Biology

, 148:769 | Cite as

High diversity of deep-sea Gromia from the Arabian Sea revealed by small subunit rDNA sequence analysis

  • Ana Aranda da Silva
  • Jan Pawlowski
  • Andrew J. Gooday
Research Article

Abstract

Gromia is a large marine protist with filose pseudopodia and ovoid test, common in coastal intertidal and sublittoral waters. Although deep-water Gromia-like morphospecies were discovered in the 1990s, their relations to the shallow water species have never been established. Moreover, very little is known about the diversity within Gromia, reflecting the fact that these morphologically relatively simple protists have few characters useful for species identification. Consequently, we have analysed the SSU rDNA and ITS rDNA genes to examine gromiid diversity in two different areas located on the Oman and Pakistan margins of the Arabian Sea (water depths 1,000–2,000 m). In total, 27 deep-sea gromiid sequences of the SSU rDNA gene and six sequences of the ITS rDNA region were obtained. Our data confirm that Gromia-like protists from the bathyal deep sea are related to the shallow-water gromiids. Within Arabian Sea Gromia, we identified seven distinctive lineages, five of which form a monophyletic group branching as a sister group to shallow-water species. Six lineages of Arabian Sea Gromia can be defined morphologically, while one lineage includes specimens that look identical to specimens from two other lineages. This indicates that each Gromia lineage represents probably a separate species and suggests that deep-sea gromiid diversity is higher than indicated by their simple morphology.

Abbreviations

bp

(Base pair)

SSU

rDNA (small subunit ribosomal DNA)

LSU

rDNA (large subunit ribosomal DNA)

ML

(Maximum likelihood)

NJ

(Neighbour-joining)

Notes

Acknowledgements

We thank the crew and officers of the RRS Charles Darwin for their skilled contribution to the collection of samples. We are grateful to the members of the scientific party on Darwin 143, 145 and 151, for helping in numerous ways at sea: Brian Bett, David Billet, Janne Kaariainen, Kate Larkin, Lisa Levin, Christine Whitcraft and Ben Wigham. We also thank all the people in the lab in Geneva that have helped us with the molecular work, in particular Cedric Berney, Fabien Burki, Jose Fahrni, Jackie Guiard-Maffia and David Longet. AAS was supported by the Portuguese FCT grant SFRH/BD/2911/2000. JP was supported by the Swiss National Science Foundation grant 3100A0–100415. Research on the Pakistan margin, including AJG was supported by the UK Natural Environment Research Council Grant NER/A/S/2000/01383. The experiments comply with current laws of the country in which the experiments were performed.

References

  1. Arnold ZM (1952) Structure and paleontological significance of the oral apparatus of the foraminiferoid Gromia oviformis Dujardin. J Paleontol 26:829–831Google Scholar
  2. Arnold ZM (1972) Observations on the biology of the protozoan Gromia oviformis Dujardin. University of California Publications in Zoology 100:1–168Google Scholar
  3. Arnold ZM (1982) Shell-wall lamination in Gromia oviformis Dujardin. J Foraminiferal Res 12:298–316CrossRefGoogle Scholar
  4. Barnett PRO, Watson J, Connelly D (1984) A multiple corer for taking virtually undisturbed samples from shelf, bathyal and abyssal sediments. Oceanologia Acta 7:399–408Google Scholar
  5. Berney C, Pawlowski J (2003) Revised small subunit rRNA analysis provides further evidence that foraminifera are related to Cercozoa. J Mol Evol 57:S120–S127PubMedCrossRefGoogle Scholar
  6. Bett BJ (2003) RRS Charles Darwin cruise 145: ecology and biogeochemistry of the Pakistan Margin. Southampton Oceanography CentreGoogle Scholar
  7. Bhattacharya D, Helmchen T, Melkonian M (1995) Molecular evolutionary analyses of nuclear-encoded small-subunit ribosomal-RNA identify an independent rhizopod lineage containing the Euglyphina and the Chlorarachniophyta. J Eukaryot Microbiol 42:65–69PubMedCrossRefGoogle Scholar
  8. Bovee EC (1985) Class Filosea Leidy, 1879. In: Lee JJ, Hutner SH, Bovee EC (eds) An illustrated guide to the protozoa. Society of Protozoologists, Kansas, pp 228–245Google Scholar
  9. Bowser SS, Marko M, Bernhard JM (1996) Occurrence of Gromia oviformis in McMurdo Sound. Antarct J US 31:122–124Google Scholar
  10. Burki F, Berney C, Pawlowski J (2002) Phylogenetic position of Gromia oviformis Dujardin inferred from nuclear-encoded small subunit ribosomal DNA. Protist 153:251–260PubMedCrossRefGoogle Scholar
  11. Cavalier-Smith T, Chao EEY (1997) Sarcomonad ribosomal RNA sequences, rhizopod phylogeny, and the origin of euglyphid amoebae. Arch Protistenkd 147:227–236Google Scholar
  12. Cavalier-Smith T, Chao EEY (2003) Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154:341–358PubMedCrossRefGoogle Scholar
  13. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  14. Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  15. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548PubMedGoogle Scholar
  16. Gooday AJ, Bowser SS, Bett BJ, Smith CR (2000) A large testate protist, Gromia sphaerica sp. nov. (Order Filosea), from the bathyal Arabian Sea. Deep Sea Res II 47:55–73CrossRefGoogle Scholar
  17. Gooday A, Bowser SS (2005) The second Gromia species (testate amoeba) from the deep sea: its natural history and association with the Pakistan margin Oxygen Minimum Zone. Protist 156:113–126 PubMedCrossRefGoogle Scholar
  18. Gooday AJ, Bowser SS, Cedhagen T, Cornelius N, Hald M, Korsun S, Pawlowski J (2005) Monothalamous foraminiferans and gromiids (Protista) from western Svalbard: a preliminary survey. Mar Biol Res 1:290–312CrossRefGoogle Scholar
  19. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  20. Hedley RH (1958) Confusion between Gromia oviformis and Allogromia ovoidea. Nature 15:1391–1392CrossRefGoogle Scholar
  21. Hedley RH (1960) The iron-containing shell of Gromia oviformis (Rhizopoda). Q J Microsc Sci 101:279–293Google Scholar
  22. Hedley RH, Bertaud WS (1962) Electron-microscopic observations of Gromia oviformis (Sarcodina). J Protozool 91:79–87Google Scholar
  23. Helly JJ, Levin LA (2004) Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Res I 51:1159–1168CrossRefGoogle Scholar
  24. Jepps MW (1926) Contribution to the study of Gromia oviformis Dujardin. Q J Microsc Sci 70:701–719Google Scholar
  25. Jumars PA (1976) Deep-sea species diversity: does it have a characteristic scale?. J Mar Res 34:217–246Google Scholar
  26. Levin L, Gage JD, Lamont PA, Cammidge L, Martin C, Patience AJ, Crooks J (1997) Infaunal community structure in a low-oxygen, organic-rich habitat on the Oman continental slope, NW Arabian Sea. In: Hawkins LE, Hutchinson S, Jensen AC, Sheader M, Williams JA (eds) 30th European marine biology symposium. The responses of marine organisms to their environments. Southampton Oceanography Centre, University of Southampton, Southampton, pp 223–230Google Scholar
  27. Longet D, Archibald JM, Keeling PJ, Pawlowski J (2003) Foraminifera and Cercozoa share a common origin according to RNA polymerase II phylogenies. Int J Syst Evol Microbiol 53:1735–1739PubMedCrossRefGoogle Scholar
  28. Longet D, Burki F, Flawkowski J, Berney C, Polet S, Fahrni J, Pawlowski J (2004) Multigene evidence for close evolutionary relations between Gromia and Foraminifera. Acta Protozoologica 43:303–311Google Scholar
  29. Neefs JM, Van de Peer Y, De Rijk P, Chapelle S, De Wachter R (1993) Compilation of small riboosmal subunit RNA structures. Nucleic Acids Res 21:3025–3049PubMedCrossRefGoogle Scholar
  30. Nikolaev SI, Berney C, Fahrni J, Mylnikov AP, Aleshin VV, Petrov NB, Pawlowski J (2003) Gymnophrys cometa and Lecythium sp. are core Cercozoa: evolutionary implications. Acta Protozoologica 42: 183–190Google Scholar
  31. Nikolaev SI, Berney C, Fahrni JF, Bolivar I, Polet S, Mylnikov AP, Aleshin VV, Petrov NB, Pawlowski J (2004) The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc Natl Acad Sci USA 101:8066–8071PubMedCrossRefGoogle Scholar
  32. Patterson DJ, Simpson A, Rogerson A (2000) Amoebae of uncertain affinities. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the Protozoa. Allen Press Inc., Lawrence Kansas, pp 804–827Google Scholar
  33. Pawlowski J, Bolivar I, Guiard-Maffia J, Gouy M (1994) Phylogenetic position of foraminifera inferred from LSU ribosomal-RNA gene-sequences. Mol Biol Evol 11:929–938PubMedGoogle Scholar
  34. Pawlowski J, Fahrni JF, Guiard J, Konlan K, Hardecker J, Habura A, Bowser SS (2005) Allogromiid foraminifera and gromiids from under the Ross Ice Shelf: morphological and molecular diversity. Polar Biol 28:514–522 CrossRefGoogle Scholar
  35. Rhumbler L (1904) Systematische Zusammenstellung der recenten Reticulosa (Nuda und Foraminifera). Arch Protistenkd 3:181–294Google Scholar
  36. Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  37. Thompson JD, Higgens DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Ana Aranda da Silva
    • 1
  • Jan Pawlowski
    • 2
  • Andrew J. Gooday
    • 1
  1. 1.National Oceanography CentreSouthamptonUK
  2. 2.Department of Zoology and Animal BiologyUniversity of GenevaGeneva 4Switzerland

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