Towards a Molecular Systematics of the Lake Baikal/Lake Tuva Sponges

  • Matthias Wiens
  • Petra Wrede
  • Vladislav A. Grebenjuk
  • Oxana V. Kaluzhnaya
  • Sergey I. Belikov
  • Heinz C. Schröder
  • Werner E. G. Müller
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 47)


Lake Baikal is famous for its extensive biodiversity that is equaled only by few other lakes. Fascinatingly, about 80% of all the animals the lake hosts are endemic. Sponges (Porifera) that live in symbiosis with photosynthetic algae are the most abundant animal taxon found in the littoral zone of Lake Baikal and have been grouped to the family Lubomirskiidae. In recent years, several attempts to determine the phylogenetic relationship between Lubomirskiidae and cosmopolitan freshwater sponges have been undertaken. Yet the results obtained remain inconclusive. Here, we strive to determine the phylogeny of freshwater sponges with the focus on endemic Lake Baikal species, also taking into account two poriferan species that were collected during an expedition in 2006 in two other isolated Siberian lakes, Lake Chagytai and Lake Tore-Khol. Since its discovery at the beginning of the twentieth century, the Lake Chagytai species was grouped to the Lubomirskiidae and called Baikalospongia dzhegatajensis. However, analyses of molecular sequence data [internal transcribed spacer 2 (ITS2), ribosomal DNA (rDNA)] and morphological markers (spicules, habitus) inferred a close relationship to the cosmopolitan genus Ephydatia and also to the Lake Tore-Khol species that had not so far been described. Thus, both species were tentatively termed Ephydatia tuva (Lake Chagytai) and E. altaiensis (Lake Tore-Khol). We hypothesize that these new species might have evolved from Ephydatia-like ancestors through adaptation to the unique environmental conditions of both lakes. To test the ITS data, an unlinked genetic locus was chosen for further phylogenetic analyses, the protein-coding gene silicatein. These analyses provided not only a more robust resolution between the Lubomirskiidae, but also corroborated the grouping of the Lake Chagytai and Lake Tore-Khol species to the genus Ephydatia. In addition, the phylogenetic analyses suggest a Spongilla-like founder generation of poriferan species in Lake Chagytai and Lake Tore-Khol. In conclusion, we propose that the process of speciation in Lake Baikal and Lake Chagytai/Lake Tore-Khol, from a cosmopolitan Spongilla-like ancestor to more than ten endemic species follows allopatric speciation patterns and is of the peripatric type.


Internal Transcribe Spacer Carbonic Anhydrase Marine Sponge Sponge Species Siliceous Sponge 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Addis JS, Petterson KJ (2005) Phylogenetic relationships of freshwater sponges (Porifera, Spongillina) inferred from analyses of 18S rDNA, COI mtDNA, and ITS2 rDNA sequences. Zool Scr 34:549–557CrossRefGoogle Scholar
  2. Annandale N (1914) Further notes on the sponges of Lake Baikal. Rec Indian Mus 10:137–148Google Scholar
  3. Bavestrello G, Arillo A, Calcinai B, Cattaneo-Vietti R, Cerrano C, Gaino E, Penna A, Sara M (2000) Parasitic diatoms inside Antarctic sponges. Biol Bull 198:29–33.CrossRefGoogle Scholar
  4. Belikov SI, Kaluzhnaya OV, Schröder HC, Krasko A, Müller IM, Müller WEG (2005) Expression of silicatein in spicules from the Baikalian sponge Lubomirskia baicalensis. Cell Biol Int 29:943–951CrossRefGoogle Scholar
  5. Bergquist PR (1978) Sponges. University of California, Berkeley, CA.Google Scholar
  6. Borchiellini C, Manuel M, Alivon E, Boury-Esnault N, Vacelet J, Le Parco Y (2001) Sponge paraphyly and the origin of Metazoa. J Evol Biol 14:171–179CrossRefGoogle Scholar
  7. Efremova SM (2001) Sponges (Porifera). In: Timoshkin OA (ed) Index of Animal Species Inhabiting Lake Baikal and Its Catchment Area. Novosibirsk Nauka, Novosibirsk, pp. 179–192Google Scholar
  8. Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753CrossRefGoogle Scholar
  9. Frost TM (1991) Porifera. In: Thorp JH, Covich AP (eds) Ecology and Classification of North American Freshwater Invertebrates. Academic, Boston, MA, pp. 95–124Google Scholar
  10. Funayama N, Nakatsukasa M, Kuraku S, Takechi K, Dohi M, Iwabe N, Miyata T, Agata K (2005) Isolation of Ef silicatein and Ef lectin as molecular markers for sclerocytes and cells involved in innate immunity in the freshwater sponge Ephydatia fluviatilis. Zool Sci 22:1113–1122CrossRefPubMedPubMedCentralGoogle Scholar
  11. Greze VN, Greze II (1958) Ozero Chagytai. Izvestija Vsesoyuznogo Geographiceskogo Obscestva 90:279–284Google Scholar
  12. Itskovich VB, Belikov SI, Efremova SM, Masuda Y (1999) Phylogenetic relationships between Lubomirskiidae, Spongillidae, and some marine sponges according to partial sequences of 18S rDNA. Mem Queensl Mus 44:275–280Google Scholar
  13. Kaluzhnaya OV, Belikov SI, Schröder HC, Rothenberger M, Zapf S, Kaandorp JA, Borejko A, Müller IM, Müller WEG (2005) Dynamics of skeleton formation in the Lake Baikal sponge Lubomirskia baicalensis. Part I: biological and biochemical studies. Naturwissenschaften 92:128–133CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kozhov M (1963) Lake Baikal and Its Life. W. Junk-Verlag, Den HaagCrossRefGoogle Scholar
  15. Kozhova OM, Izmest'eva LR (1998) Lake Baikal — Evolution and Biodiversity. Backhys, LeidenGoogle Scholar
  16. Kruse M, Gamulin V, Cetkovic H, Pancer Z, Müller IM, Müller WEG (1996) Molecular evolution of the metazoan protein kinase C multigene family. J Mol Evol 43:374–383CrossRefGoogle Scholar
  17. Lafay B, Boury-Esnault N, Vacelet J, Christen R (1992) An analysis of partial 28S ribosomal RNA sequences suggests early radiations of sponges. Biosystems 28:139–151CrossRefGoogle Scholar
  18. Manconi R, Pronzato R (2002) Suborder Spongillina subord. nov: Freshwater sponges. In: Hooper JNA, van Soest RWM (eds) Systema Porifera: A Guide to the Classification of Sponges. Kluwer, New York, pp. 921–1019Google Scholar
  19. Masuda Y, Itskovich VB, Veinberg EV, Efremova SM (1997) Studies on the taxonomy and distribution of freshwater sponges in the Lake Baikal. In: Miyzaki N (ed) Animal Community, Environment and Phylogeny in Lake Baikal. Otsuchi Marine Center/Ocean Research Institute, Tokyo, Japan, pp. 25–33Google Scholar
  20. Meixner MJ, Lüter C, Eckert C, Itskovich V, Janussen D, von Rintelen T, Bohne AV, Meixner JM, Hess WR (2007) Phylogenetic analysis of freshwater sponges provide evidence for endemism and radiation in ancient lakes. Mol Phylogent Evol 45:875–886CrossRefGoogle Scholar
  21. Müller WEG (1995) Molecular phylogeny of metazoa [Animals]. Monophyletic origin. Naturwissen-schaften 82:321–329CrossRefGoogle Scholar
  22. Müller WEG (2001) How was the metazoan threshold crossed? The hypothetical Urmetazoa. Comp Biochem Physiol (A) 129:433–460CrossRefGoogle Scholar
  23. Müller WEG, Müller I, Zahn RK, Maidhof A (1984) Intraspecific recognition system in scle-ractinian corals: morphological and cytochemical description of the autolysis mechanism. J Histochem Cytochem 32:285–288CrossRefGoogle Scholar
  24. Müller WEG, Schröder HC, Skorokhod A, Bünz C, Müller IM, Grebenjuk VA (2001) Contribution of sponge genes to unravel the genome of the hypothetical ancestor of Metazoa (Urmetazoa). Gene 276:161–173CrossRefGoogle Scholar
  25. Müller WEG, Brümmer F, Batel R, Müller IM, Schröder HC (2003) Molecular biodiversity. Case study: Porifera (sponges). Naturwissenschaften 90:103–120CrossRefGoogle Scholar
  26. Müller WEG, Schröder HC, Wrede P, Kaluzhnaya OV, Belikov SI (2006) Speciation of sponges in Baikal-Tuva region (an outline). J Zool Syst Evol Res 44:105–117CrossRefGoogle Scholar
  27. Müller WEG, Boreiko A, Wang X, Belikov SI, Wiens M, Grebenjuk VA, Schloßmacher U, Schröder HC (2007a) Silicateins, the major biosilica forming enzymes present in demos-ponges: protein analysis and phylogenetic relationship. Gene 395:62–71CrossRefGoogle Scholar
  28. Müller WEG, Schloßmacher U, Eckert C, Krasko A, Boreiko A, Ushijima H, Wolf SE, Tremel W, Schröder HC (2007b) Analysis of the axial filament in spicules of the demosponge Geodia cydonium: different silicatein composition in microscleres [asters] and megascleres [oxeas and triaenes]. Eur J Cell Biol 86:473–487CrossRefGoogle Scholar
  29. Müller WEG, Boreiko A, Wang X, Belikov SI, Wiens M, Grebenjuk VA, Schlossmacher U, Schröder HC (2007c) Silicateins, the major biosilica forming enzymes present in demos-ponges: protein analysis and phylogenetic relationship. Gene 395:62–71CrossRefGoogle Scholar
  30. Müller WEG, Schröder HC, Belikov SI (2008a) Sustainable exploitation and conservation of the endemic Lake Baikal sponge (Lubomirskia baicalensis) for the application in nanobiotechnol-ogy. In: Müller WEG, Grachev MA (eds) Potential of Biosilica in Evolution, Morphogenesis and Nanobiotechnology. Springer-Verlag, HeidelbergGoogle Scholar
  31. Müller WEG, Wang X, Kropf K, Boreiko A, Schloßmacher U, Brandt D, Schröder HC, Wiens M (2008b) Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges. Cell Tissue Res: Epub ahead of print.Google Scholar
  32. Nakamura Y, Sato S, Kaneko T, Kotani H, Asamizu E, Miyajima N, Tabata S (1997) Structural analysis of Arabidopsis thaliana chromosome 5. III. Sequence features of the regions of 1,191,918 bp covered by seventeen physically assigned P1 clones. DNA Res 4:401–414CrossRefPubMedPubMedCentralGoogle Scholar
  33. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217CrossRefGoogle Scholar
  34. Ovchinnikova NS (ed) (2005) Atlas of Lake Baikal; Past-Present-Future. Omskaya Kartographich-eskaya Fabr, OmskGoogle Scholar
  35. Pallas PS (1776) Reise durch die verschiedenen Provinzen des Russischen Reiches. St. PetersburgGoogle Scholar
  36. Pfeifer K, Haasemann M, Gamulin V, Bretting H, Fahrenholz F, Müller WEG (1993) S-type lectins occur also in invertebrates: unusual subunit composition and high conservation of the carbohydrate recognition domain in the lectin genes from the marine sponge Geodia cydo-nium. Glycobiology 3:179–184CrossRefGoogle Scholar
  37. Popovskaya GI, Genkal SI, Likhoshway YV (2002) Diatoms of the Plankton of Lake Baikal. Nauka, NovosibirskGoogle Scholar
  38. Rezvoj PD (1927) Notes on sponges from the Lake Dzhegataj-kul in the Urjankhaj region. Doklady Akademii Naukk SSSR 3/8:296–300Google Scholar
  39. Rezvoj PD (1936) Freshwater sponges of the USSR. In: Rezvoj PD (ed) The Fauna of the USSR. Academy of Sciences, Moscow, Leningrad, pp. 1–42Google Scholar
  40. Rodrigo AG, Bergquist PR, Bergquist PL, Reeves RA (1994) Are sponges animals: an investigation into the vagaries of phylogenetic inferences. In: Soest RW, Kempen TMG, Braekman, JC (eds) Sponges in Time and Space. Balkema, Rotterdam, pp. 47–54.Google Scholar
  41. Savarese M, Patterson MR, Chernykh VI, Fialkov VA (1997) Trophic effects of sponge feeding within Lake Baikal's littoral zone. 1. In situ pumping rate. Limnol Oceanogr 42:171–178CrossRefGoogle Scholar
  42. Schröder HC, Efremova SM, Itskovich VB, Belikov S, Masuda Y, Krasko A, Müller IM, Müller WEG (2003a) Molecular phylogeny of the freshwater sponges in Lake Baikal. J Zoolog Syst Evol Res 41:80–86CrossRefGoogle Scholar
  43. Schröder HC, Krasko A, Le Pennec G, Adell T, Hassanein H, Müller IM, Müller WEG (2003b) Silicase, an enzyme which degrades biogenous amorphous silica: contribution to the metabolism of silica deposition in the demosponge Suberites domuncula. Prog Mol Subcell Biol 33:249–268CrossRefGoogle Scholar
  44. Schröder HC, Perovic-Ottstadt S, Rothenberger M, Wiens M, Schwertner H, Batel R, Korzhev M, Müller IM, Müller WEG (2004) Silica transport in the demosponge Suberites domuncula: fluorescence emission analysis using the PDMPO probe and cloning of a potential transporter. Biochem J 381:665–673CrossRefPubMedPubMedCentralGoogle Scholar
  45. Schröder HC, Brandt D, Schlossmacher U, Wang X, Tahir MN, Tremel W, Belikov SI, Müller WEG (2007) Enzymatic production of biosilica glass using enzymes from sponges: basic aspects and application in nanobiotechnology (material sciences and medicine). Naturwissenschaften 94:339–359.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Schulze P (1923) Beiträge zur Kenntnis der Kieselnadelbildung besonders bei den Spongilliden. Arch f Zellforsch 17:105–130Google Scholar
  47. Sherbakov DY (1999) Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends Ecol Evol 14:92–95CrossRefGoogle Scholar
  48. Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA 95:6234–6238CrossRefGoogle Scholar
  49. Simon L (1955) Über ökologische Typenbildung bei Süsswasserschwämmen. Arch f Hydrobiol 50:136–140Google Scholar
  50. Simpson TL, Garrone R, Mazzorana M (1983) Interaction of germanium (Ge) with biosilicifica-tion in the freshwater sponge Ephydatia muelleri: evidence of localized membrane domains in the silicalemma. J Ultrastruct Res 85:159–174CrossRefPubMedPubMedCentralGoogle Scholar
  51. Uriz MJ, Turon X, Becerro MA, Agell G (2003) Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions. Microsc Res Tech 62:279–299CrossRefPubMedPubMedCentralGoogle Scholar
  52. Volkel H, Kurz U, Linder J, Klumpp S, Gnau V, Jung G, Schultz JE (1996) Cathepsin L is an intra-cellular and extracellular protease in Paramecium tetraurelia. Purification, cloning, sequencing and specific inhibition by its expressed propeptide. Eur J Biochem 238:198–206CrossRefPubMedPubMedCentralGoogle Scholar
  53. Waller JG (1878) On variation in Spongilla lacustris. J Quekett Microsc Club 5:53–62Google Scholar
  54. Weaver J, Morse DE (2003) Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech 62:356–367CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wiens M, Müller WEG (2006) Cell death in Porifera: molecular players in the game of apoptotic cell death in living fossils. Can J Zool 84:307–332CrossRefGoogle Scholar
  56. Wiens M, Belikov SI, Kaluzhnaya OV, Krasko A, Schröder HC, Perovic-Ottstadt S, Müller WEG (2006) Molecular control of serial module formation along the apical-basal axis in the sponge Lubomirskia baicalensis: silicateins, mannose-binding lectin and mago nashi. Dev Genes Evol 216:229–242CrossRefGoogle Scholar
  57. Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S, Müller WEG (2007) Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Mol Biol Evol 24:792–804CrossRefPubMedPubMedCentralGoogle Scholar
  58. Wiens M, Grebenjuk VA, Schröder HC, Müller WEG (2008) Identification and isolation of a retrotransposon from the Lubomirskia baicalensis: implication in rapid evolution of endemic sponges. In: Müller WEG, Grachev MA (eds) Potential of Biosilica in Evolution, Morphogenesis and Nanobiotechnology. Springer-Verlag, HeidelbergGoogle Scholar
  59. Wörheide G, Nichols SA, Goldberg J (2004) Intragenomic variation of the rDNA internal transcribed spacers in sponges (Phylum Porifera): implications for phylogenetic studies. Mol Phylogenet Evol 33:816–830.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  • Matthias Wiens
    • 1
  • Petra Wrede
    • 1
  • Vladislav A. Grebenjuk
    • 1
  • Oxana V. Kaluzhnaya
    • 2
  • Sergey I. Belikov
    • 2
  • Heinz C. Schröder
    • 1
  • Werner E. G. Müller
    • 1
    • 1
  1. 1.Institut für Physiologische Chemie, Abteilung Angewandte Molekularbiologie, UniversitätMainzGermany
  2. 2.Limnological Institute of the Siberian Branch of Russian Academy of SciencesIrkutskRussia

Personalised recommendations