Abstract
Komokiaceans are testate agglutinated protists, extremely diverse and abundant in the deep sea. About 40 species are described and share the same main morphological feature: a test consisting of narrow branching tubules forming a complex system. In some species, the interstices between the tubules are filled by sediment, creating a mudball structure. Because of their unusual and sometimes featureless appearance, komokiaceans were frequently ignored or overlooked until they formal description in 1977. The most recent taxonomy places the Komokiacea within the Foraminifera based on general morphological features. To examine their taxonomic position at the molecular level, we analysed the SSU rDNA sequences of two species, Normanina conferta and Septuma ocotillo, obtained either with specific foraminiferal or universal eukaryotic primers. Many different sequences resulted from this investigation but none of them could clearly be attributed to komokiaceans. Although our study failed to confirm univocally that Komokiacea are foraminiferans, it revealed a huge eukaryotic richness associated with these organisms, comparable with the richness in the overall surrounding sediment. These observations suggest strongly that komokiaceans, and probably many other large testate protists, provide a habitat structure for a large spectrum of eukaryotes, significantly contributing to maintaining the biodiversity of micro- and meiofaunal communities in the deep sea.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Bilofsky HS, Burks C, Fickett JW, Goad WB, Lewitter FI, Rindone WP, Swindell CD, Tung CS (1986) The GenBank genetic sequence databank. Nucleic Acids Res 14:1–4 doi:10.1093/nar/14.1.1
Bowser SS, Habura A, Pawlowski J (2006) Molecular evolution of foraminifera. In: Katz L, Bhattacharya D (eds) Genomics and evolution of microbial eukaryotes. Oxford University Press, New York, pp 78–93
Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354
Damare S, Raghukumar C, Raghukumar S (2006) Spore germination of fungi belonging to Aspergillus species under deep-sea conditions. Deep Sea Res Part I Oceanogr Res Pap 55:670–678 doi:10.1016/j.dsr.2008.02.004
Dawson SC, Pace NR (2002) Novel kingdom-level eukaryotic diversity in anoxic environment. Proc Natl Acad Sci USA 99:8324–8329 doi:10.1073/pnas.062169599
Edgcomb VP, Kysela DT, Teske A, De Vera Gomez A, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci USA 99:7658–7662 doi:10.1073/pnas.062186399
Epstein S, Lopez-Garcia P (2008) “Missing” protists: a molecular perspective. Biodivers Conserv 17:261–276 doi:10.1007/s10531-007-9250-y
Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN, two graphic tools for sequence alignment and molecular phylogeny. CABIOS 12:543–548
Gooday AJ, Cook PL (1984) An association between komokiacean foraminiferans (Protozoa) and paludicelline ctenostomes (Bryozoa) from the abyssal northeast Atlantic. J Nat Hist 18:765–784 doi:10.1080/00222938400770641
Gooday AJ, Levin LA, Thomas CL, Hecker B (1992) The taxonomy, distribution and ecology of Bathysiphon filiformis and B. major (Protista, Foraminiferida) on the continental slope off North Carolina. J Foraminiferal Res 22:129–146
Gooday AJ, Holzmann M, Guiard J, Cornelius N, Pawlowski J (2004) A new monothalamous foraminiferan from 1000–6300 m water depth in the Weddell Sea: morphological and molecular characterization. Deep Sea Res Part II 51:1603–1616
Gooday AJ, Kamenskaya OE, Cedhagen T (2007a) New and little-known Komokiacea (Foraminifera) from the bathyal and abyssal Weddell Sea and adjacent areas. Zool J Linn Soc 151:219–251 doi:10.1111/j.1096-3642.2007.00326.x
Gooday AJ, Cedhagen T, Kamenskaya OE, Cornelius N (2007b) The biodiversity and biogeography of komokiaceans and other enigmatic foraminiferan-like protists in the deep Southern Ocean. Deep Sea Res Part II Top Stud Oceanogr 54:1691–1719 doi:10.1016/j.dsr2.2007.07.003
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 doi:10.1080/10635150390235520
Hessler RR, Jumars PA (1974) Abyssal community analysis from replicate box cores in the central North Pacific. Deep Sea Res 21:185–209
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755 doi:10.1093/bioinformatics/17.8.754
Hughes JA, Gooday AJ (2004) The influence of dead Syringammina fragilissima (Xenophyophorea) tests on the distribution of benthic foraminifera in the Darwin Mounds region (NE Atlantic). Deep Sea Res Part I Oceanogr Res Pap 51:1741–1758
Jumars PA, Gallagher ED (1982) Deep-sea community structure: tree plays on the benthic proscenium. In: Ernst WG, Morin JG (eds) The environment of the deep sea. Prentice-Hall, Englewood Cliffs, pp 217–255
Kamenskaya OE (2000) Order Komokiida. In Alimov AF (ed) Protista: Manual on Zoology, Part 1. Nauka, St. Petersburg, pp 524–527
Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20:670–676 doi:10.1016/j.tree.2005.09.005
Levin LA (1991) Interactions between metazoans and large, agglutinated protozoans: implications for the community structure of deep-sea benthos. Am Zool 31:886–900
Levin LA, Thomas CL (1988) The ecology of xenophyophores (Protista) on eastern Pacific seamounts. Deep-Sea Res 35:2003–2027 doi:10.1016/0198-0149(88)90122-7
Lopez-Garcia P, Rodriguez-Valera F, Pedro-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607 doi:10.1038/35054537
Moodley L, Middelburg JJ, Boschker HTS, Duineveld GCA, Pel R, Herman PMJ, Heip CHR (2002) Bacteria and Foraminifera: key players in a short-term deep-sea benthic response to phytodetritus. Mar Ecol Prog Ser 236:23–29 doi:10.3354/meps236023
Norman AM (1978) On the genus Haliphysema, with the description of several forms apparently allied to it. Annals and Magazine of Natural History series 5 1:264–284
Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ (2007) Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol 9:1233–1252 doi:10.1111/j.1462-2920.2007.01247.x
Pawlowski J (2000) Introduction to the molecular systematics of foraminifera. Micropaleontology 46(Suppl 1):1–12
Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences using computer simulations. Proc Natl Acad Sci USA 98:13757–13762 doi:10.1073/pnas.241370698
Sanders HL, Hessler RR, Hampson GR (1965) An introduction to the study of the deep-sea benthic faunal assemblages along the Gay Head, Bermuda transect. Deep Sea Res 12:845–867
Schröder CJ, Medioli FS, Scott DB (1989) Fragile abyssal foraminifera (including new Komokiacea) from the Nares abyssal plain. Micropaleontology 35:10–48 doi:10.2307/1485535
Shires R, Gooday AJ, Jones AR (1994) A new large agglutinated foraminifer (Arboramminidae n. fam.) from a oligotrophic site in the abyssal northeast Atlantic. J Foraminiferal Res 24:149–157
Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T (2007) Diversity of microbial eukaryotes in sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples and two enrichment cultures. Extremophiles 11:563–576 doi:10.1007/s00792-007-0068-z
Tendal OS (1979) Aspects of the biology of Komokiacea and Xenophyophoria. Sarsia 64:13–17
Tendal OS, Hessler RR (1977) An introduction to the biology and systematics of Komokiacea (Textulariina, Foraminiferida). Galathea Rep 14:165–194
Thiel H, Pfannkuche O, Schriever G, Lochte K, Gooday AJ, Hemleben C, Mantoura RFC, Turley CM, Patching JW, Riemann F (1989) Phytodetritus on the deep-sea floor in a central oceanic region of the northeast Atlantic. Biol Oceanogr 6:203–239
Vickerman K (1992) The diversity and ecological significance of Protozoa. Biodivers Conserv 1:334–341
Acknowledgements
We thank A. Brandt, B. Hilbig, D. Fütterer, E. Fahrbach, and the Captain, officers and crew of the Polarstern for their assistance during the ANDEEP II and III expeditions. We also thank J. Blake for collecting komoki using elutriation technique during “ANDEEP II” expedition. This study was supported by the Swiss National Science Foundation (grant no. 3100A0-112645 to J.P.), the Danish Research Agency (Grant no. 95091435 to T.C.), and the UK Natural Environment Research Council (Grant no. NER/B/S/2001/00336 to A.J.G.). This is ANDEEP publication no. 119. This publication also contributes to the CoML field project CeDAMar.
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Lecroq, B., Gooday, A.J., Cedhagen, T. et al. Molecular analyses reveal high levels of eukaryotic richness associated with enigmatic deep-sea protists (Komokiacea). Mar Biodiv 39, 45–55 (2009). https://doi.org/10.1007/s12526-009-0006-7
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DOI: https://doi.org/10.1007/s12526-009-0006-7