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Elucidation of phylogenetic processes during early evolution of basal Metazoa through the phylogenetic study of both, selected molecular marker genes and EST data

Subject Area Evolution, Anthropology
Term from 2005 to 2009
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 5453326
 
Final Report Year 2009

Final Report Abstract

The phylogeny of early-branching Metazoa and the origin of animal life have been subject to unrelenting controversies since inferences from morphological and molecular analyses are frequently conflicting. Uncertainty not only surrounds the interrelationship between metazoan phyla (i.e. the relative topology of Porifera, Cnidaria, Ctenophora, and Bilateria) but also on many other systematic levels relationships remain unresolved (e.g. monophyly/paraphyly of Porifera and poriferan classes, evolutionary origin of freshwater sponges). Since most phylogenetic conflicts are the result of poorly sampled taxa that tend to be unstable and obscure strongly supported relationships between stable taxa, we aimed to generate a robust phylogenetic framework. This framework is a fundamental requirement to analyze the deepest splits in the animal tree of life and, consequently, to understand the evolution of animal diversity. Accordingly, new cDNA libraries and "expressed sequence tags" (ESTs) for six representatives of all poriferan classes (and respective "subclasses") were generated, including previously unsampled or poorly sampled but pivotal taxa. In addition, an extensive matrix of molecular markers (protein coding genes, ITS) was established, comprising species of Porifera, Cnidaria, Choanoflagellata. Moreover, to facilitate both bioinformatic processing of the vast amount of sequence data and data mining, the combination of a BioPerl-based pipeline and a MySQL-based multithreaded database was designed. Ultimately, these processed data have provided new insight into the topology of basal metazoan taxa: They strongly corroborate the monophyly of Porifera, the sister-group relationship of Choanoflagellata and Metazoa, and the monophyly of Demospongiae "sensu stricto" and Hexactinellida. In combination with morphological markers the data also allowed to investigate the phylogeny of endemic demosponges of ancient lakes and their close relationship to certain cosmopolitan demosponge species. In addition, analyses of the demospongian mitochondrial genome, which is so far the largest in size found in sponges, confirmed the close relationship between Porifera and Choanoflagellata. Furthermore, the evolution of the metazoan-specific genetic toolkit was analyzed. Thus, receptors, ligands, adapters, regulators, effectors, and transcription factors involved in pathways of apoptosis, innate immunity, morphogenesis, and spiculogenesis were discovered and phylogenetically characterized with respect to both sequence and function. Finally, for the first time, molecular evidence was provided for the existence of both a poriferan bioluminescence-generating enzyme and a photosensory system. The latter one is based on cryptochromes (evolutionarily old and highly conserved flavoproteins), which are pivotal in the generation and maintenance of metazoan circadian rhythms.

Publications

  • 2006. Axial (apical-basal) expression of pro-apoptotic and pro-survival genes in the Lake Baikal demosponge Lubomirskia baicalensis. DNA and Cell Biology, Vol. 25. 2006, Issue 3, pp. 152-164.
    Wiens M., Belikov S.I., Kaluzhnaya O.V., Schröder H.C., Hamer B., Perovic-Ottstadt S., Boreiko A., Luthringer B., Müller I.M., Müller W.E.G.
    (See online at https://dx.doi.org/10.1089/dna.2006.25.152)
  • Silicateins, the major biosilica forming enzymes present in demosponges: protein analysis and phylogenetic relationship. Gene, Vol. 395. 2007, Issues 1–2, pp. 62–71.
    Müller W.E., Boreiko A., Wang X., Belikov S.I., Wiens M., Grebenjuk V.A., Schlossmacher U., Schröder H.C.
    (See online at https://dx.doi.org/10.1016/j.gene.2007.02.014)
  • Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Molecular Biology and Evolution, Vol. 24. 2007, Issue 3, Pp. 792-804.
    Wiens M., Korzhev M., Perovic-Ottstadt S., Luthringer B., Brandt D., Klein S., Müller W.E.G.
    (See online at https://dx.doi.org/10.1093/molbev/msl208)
  • Mitochondrial genome of Suberites domuncula: Palindromes and inverted repeats are abundant in non-coding regions. Gene, Vol. 412. 2008, Issues 1–2, pp. 1–11.
    Lukić-Bilela L., Brandt D., Pojskić N., Wiens M., Gamulin V., Müller W.E.G.
    (See online at https://dx.doi.org/10.1016/j.gene.2008.01.001)
  • Regional and modular expression of morphogenetic factors in the demosponge Lubomirskia baicalensis. Micron, Vol. 39. 2008, Issue 4, pp. 447–460.
    Wiens M., Belikov S.I., Kaluzhnaya O.V., Adell T., Schröder H.C., Perovic-Ottstadt S., Kaandorp J.A., Müller W.E.G.
    (See online at https://dx.doi.org/10.1016/j.micron.2007.02.003)
  • Silicatein expression in the hexactinellid Crateromorpha meyeri: the lead marker gene restricted to siliceous sponges. Cell and Tissue Research, Volume 333. 2008, Issue 2, pp. 339-351.
    Müller W.E.G., Wang X., Kropf K., Boreiko A., Schlossmacher U., Brandt D., Schröder H.C., Wiens M.
    (See online at https://dx.doi.org/10.1007/s00441-008-0624-6)
  • The 2'-5'-oligoadenylate synthetase in the lowest metazoa: isolation, cloning, expression and functional activity in the sponge Lubomirskia baicalensis. Molecular Immunology, Vol. 45. 2008, Issue 4, pp. 945–953.
    Schröder H.C., Natalio F., Wiens M., Tahir M.N., Shukoor M.I., Tremel W., Belikov S.I., Krasko A., Müller W.E.G.
    (See online at https://dx.doi.org/10.1016/j.molimm.2007.07.036)
  • Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society B: Biological Sciences, Vol. 276. 2009, issue 1677, pp. 4261-4270.
    Hejnol A., Obst M., Stamatakis A., Ott M., Rouse G.W., Edgecombe G.D., Martinez P., Baguna J., Bailly X., Jondelius U., Wiens M., et al.
    (See online at https://dx.doi.org/10.1098/rspb.2009.0896)
  • Identification and isolation of a retrotransposon from the freshwater sponge Lubomirskia baicalensis: implication in rapid evolution of endemic sponges. In: W.E.G. Müller, M.A. Grachev(eds), Biosilica in Evolution, Morphogenesis, and Nanobiotechnology. Progress in Molecular and Subcellular Biology, Vol. 47.2009, pp 207-234.
    Wiens M., Grebenjuk V.A., Schröder H.C., Müller I.M., Müller W.E.G.
    (See online at https://dx.doi.org/10.1007/978-3-540-88552-8_9)
  • Luciferase a light source for the silica-based optical waveguides (spicules) in the demosponge Suberites domuncula. Cellular and Molecular Life Sciences, Vol. 66. 2009, Issue 3, pp. 537-552.
    Müller W.E.G., Kasueske M., Wang X., Schröder H.C., Wang Y., Pisignano D., Wiens M.
    (See online at https://dx.doi.org/10.1007/s00018-008-8492-5)
  • The role of the silicatein-alpha interactor silintaphin-1 in biomimetic biomineralization. Biomaterials, Vol. 30. 2009, Issue 8, pp. 1648–1656.
    Wiens M., Bausen M., Natalio F., Link T., Schlossmacher U., Müller W.E.G.
    (See online at https://dx.doi.org/10.1016/j.biomaterials.2008.12.021)
  • 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 Nanobiology. Progress in Molecular and Subcellular Biology, Vol. 47.2009, pp 111-144.
    Wiens M., Wrede P., Grebenjuk V.A., Kaluzhnaya O.V., Belikov S.I., Schröder H.C., Müller W.E.G.
    (See online at https://dx.doi.org/10.1007/978-3-540-88552-8_5)
  • A cryptochrome-based photosensory system in the siliceous sponge Suberites domuncula (Demospongiae). FEBS Journal, Vol. 277. 2010, Issue 5, pp. 1182–1201.
    Müller W.E.G., Wang X., Schröder H.C., Korzhev M., Grebenjuk V.A., Markl J.S., Jochum K.P., Pisignano D., Wiens M.
    (See online at https://dx.doi.org/10.1111/j.1742-4658.2009.07552.x)
  • Flashing light signaling circuit in sponges: endogenous light generation after tissue ablation in Suberites domuncula. Journal of Cellular Biochemistry, Vol. 111. 2010, Issue 6, pp. 1377–1389.
    Wiens M., Wang X., Unger A., Schröder H.C., Grebenjuk V.A., Pisignano D., Jochum K.P., Müller W.E.G.
    (See online at https://dx.doi.org/10.1002/jcb.22866)
  • Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol. 2010. 27:1983-1987 Molecular Biology and Evolution, Vol. 27. 2010, Issue 9, pp. 1983-1987.
    Pick K.S., Philippe H., Schreiber F., Erpenbeck D., Jackson D.J., Wrede P., Wiens M., Alié A., Morgenstern B., Manuel M., Wörheide G.
    (See online at https://dx.doi.org/10.1093/molbev/msq089)
  • Poriferan survivin exhibits a conserved regulatory role in the interconnected pathways of cell cycle and apoptosis. Cell Death and Differentiation, Vol. 18. 2011, pp. 201–213.
    Luthringer B., Isbert S., Thakur N.L., Kelve M., Müller W.E.G., Wiens M.
    (See online at https://dx.doi.org/10.1038/cdd.2010.87)
 
 

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