Skip to main content

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

  • Chapter
  • First Online:
Biosilica in Evolution, Morphogenesis, and Nanobiotechnology

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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 34:549–557

    Article  Google Scholar 

  • Annandale N (1914) Further notes on the sponges of Lake Baikal. Rec Indian Mus 10:137–148

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 29:943–951

    Article  CAS  PubMed  Google Scholar 

  • Bergquist PR (1978) Sponges. University of California, Berkeley, CA.

    Google Scholar 

  • 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 14:171–179

    Article  CAS  PubMed  Google Scholar 

  • Efremova SM (2001) Sponges (Porifera). In: Timoshkin OA (ed) Index of Animal Species Inhabiting Lake Baikal and Its Catchment Area. Novosibirsk Nauka, Novosibirsk, pp. 179–192

    Google Scholar 

  • Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753

    Article  CAS  PubMed  Google Scholar 

  • Frost TM (1991) Porifera. In: Thorp JH, Covich AP (eds) Ecology and Classification of North American Freshwater Invertebrates. Academic, Boston, MA, pp. 95–124

    Google Scholar 

  • 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 22:1113–1122

    Article  CAS  Google Scholar 

  • Greze VN, Greze II (1958) Ozero Chagytai. Izvestija Vsesoyuznogo Geographiceskogo Obscestva 90:279–284

    Google Scholar 

  • 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 44:275–280

    Google Scholar 

  • 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 92:128–133

    Article  CAS  PubMed  Google Scholar 

  • Kozhov M (1963) Lake Baikal and Its Life. W. Junk-Verlag, Den Haag

    Book  Google Scholar 

  • Kozhova OM, Izmest'eva LR (1998) Lake Baikal — Evolution and Biodiversity. Backhys, Leiden

    Google Scholar 

  • 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 43:374–383

    Article  CAS  PubMed  Google Scholar 

  • Lafay B, Boury-Esnault N, Vacelet J, Christen R (1992) An analysis of partial 28S ribosomal RNA sequences suggests early radiations of sponges. Biosystems 28:139–151

    Article  CAS  PubMed  Google Scholar 

  • 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. 921–1019

    Google Scholar 

  • 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. 25–33

    Google Scholar 

  • 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 45:875–886

    Article  CAS  Google Scholar 

  • Müller WEG (1995) Molecular phylogeny of metazoa [Animals]. Monophyletic origin. Naturwissen-schaften 82:321–329

    Article  Google Scholar 

  • Müller WEG (2001) How was the metazoan threshold crossed? The hypothetical Urmetazoa. Comp Biochem Physiol (A) 129:433–460

    Article  Google Scholar 

  • 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 32:285–288

    Article  PubMed  Google Scholar 

  • 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 276:161–173

    Article  PubMed  Google Scholar 

  • Müller WEG, Brümmer F, Batel R, Müller IM, Schröder HC (2003) Molecular biodiversity. Case study: Porifera (sponges). Naturwissenschaften 90:103–120

    Article  CAS  PubMed  Google Scholar 

  • 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 44:105–117

    Article  Google Scholar 

  • 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 395:62–71

    Article  CAS  PubMed  Google Scholar 

  • 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 86:473–487

    Article  CAS  PubMed  Google Scholar 

  • 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 395:62–71

    Article  CAS  PubMed  Google Scholar 

  • 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, Heidelberg

    Google Scholar 

  • 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 

  • 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 4:401–414

    Article  CAS  PubMed  Google Scholar 

  • Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217

    Article  CAS  PubMed  Google Scholar 

  • Ovchinnikova NS (ed) (2005) Atlas of Lake Baikal; Past-Present-Future. Omskaya Kartographich-eskaya Fabr, Omsk

    Google Scholar 

  • Pallas PS (1776) Reise durch die verschiedenen Provinzen des Russischen Reiches. St. Petersburg

    Google Scholar 

  • 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 3:179–184

    Article  CAS  PubMed  Google Scholar 

  • Popovskaya GI, Genkal SI, Likhoshway YV (2002) Diatoms of the Plankton of Lake Baikal. Nauka, Novosibirsk

    Google Scholar 

  • Rezvoj PD (1927) Notes on sponges from the Lake Dzhegataj-kul in the Urjankhaj region. Doklady Akademii Naukk SSSR 3/8:296–300

    Google Scholar 

  • Rezvoj PD (1936) Freshwater sponges of the USSR. In: Rezvoj PD (ed) The Fauna of the USSR. Academy of Sciences, Moscow, Leningrad, pp. 1–42

    Google Scholar 

  • 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 

  • 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 42:171–178

    Article  Google Scholar 

  • 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 41:80–86

    Article  Google Scholar 

  • 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 33:249–268

    Article  PubMed  Google Scholar 

  • 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 381:665–673

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Schulze P (1923) Beiträge zur Kenntnis der Kieselnadelbildung besonders bei den Spongilliden. Arch f Zellforsch 17:105–130

    Google Scholar 

  • Sherbakov DY (1999) Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends Ecol Evol 14:92–95

    Article  Google Scholar 

  • Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein alpha: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA 95:6234–6238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon L (1955) Über ökologische Typenbildung bei Süsswasserschwämmen. Arch f Hydrobiol 50:136–140

    Google Scholar 

  • 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 85:159–174

    Article  CAS  PubMed  Google Scholar 

  • 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 62:279–299

    Article  CAS  PubMed  Google Scholar 

  • 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 238:198–206

    Article  CAS  PubMed  Google Scholar 

  • Waller JG (1878) On variation in Spongilla lacustris. J Quekett Microsc Club 5:53–62

    Google Scholar 

  • Weaver J, Morse DE (2003) Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech 62:356–367

    Article  CAS  PubMed  Google Scholar 

  • Wiens M, Müller WEG (2006) Cell death in Porifera: molecular players in the game of apoptotic cell death in living fossils. Can J Zool 84:307–332

    Article  CAS  Google Scholar 

  • 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 216:229–242

    Article  CAS  PubMed  Google Scholar 

  • 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 24:792–804

    Article  CAS  PubMed  Google Scholar 

  • 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, Heidelberg

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Wiens, M. et al. (2009). Towards a Molecular Systematics of the Lake Baikal/Lake Tuva Sponges. In: Müller, W.E.G., Grachev, M.A. (eds) Biosilica in Evolution, Morphogenesis, and Nanobiotechnology. Progress in Molecular and Subcellular Biology, vol 47. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88552-8_5

Download citation

Publish with us

Policies and ethics