Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-18T08:30:25.925Z Has data issue: false hasContentIssue false
  • English
  • Français

The lysidyl aminoacyl transfer RNA synthetase intron, a new marker for demosponge phylogeographics – case study on Neopetrosia

Published online by Cambridge University Press:  12 November 2015

Edwin Setiawan ,
Nicole J. De Voogd ,
John N.A. Hooper ,
Gert Wörheide  and
Dirk Erpenbeck
Edwin Setiawan
Affiliation:
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-University Munich, Munich, Germany Zoology Lab, Biology Department, Mathematic and Natural Science Faculty, Sepuluh November Institute of Technology, Surabaya, Indonesia Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, the Netherlands
Nicole J. De Voogd
Affiliation:
Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, the Netherlands
John N.A. Hooper
Affiliation:
Biodiversity Program, Queensland Museum, South Brisbane, Australia Eskitis Institute for Drug Discovery, Griffith University, Nathan, Queensland 4111, Australia
Gert Wörheide
Affiliation:
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-University Munich, Munich, Germany GeoBio-Center LMU Ludwig-Maximilians-University Munich, Richard-Wagner-Str. 10, 80333 Munich, Germany SNSB – Bayerische Staatssammlung für Paläontologie und Geologie, Munich 80333, Germany
Dirk Erpenbeck*
Affiliation:
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-University Munich, Munich, Germany GeoBio-Center LMU Ludwig-Maximilians-University Munich, Richard-Wagner-Str. 10, 80333 Munich, Germany
*
Correspondence should be addressed to:D. Erpenbeck, Department of Earth and Environmental Sciences & GeoBio-Center LMU, Ludwig-Maximilians-University Munich, Richard-Wagner-Str. 10, 80333 Munich, Germany Email: erpenbeck@lmu.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Suitable genetic markers for population studies in sponges are necessary to further our understanding of biodiversity and dispersal patterns, and contribute to conservation efforts. Due to the slow mitochondrial substitution rates in demosponges, nuclear introns are among the preferable markers for phylogeographic studies, but so far only the second intron of the ATP synthetase beta subunit-gene (ATPSβ) has been successfully established. In the present study, we analyse the intron of the Lysidyl Aminoacyl Transfer RNA Synthetase (LTRS), another potential marker to study demosponge intraspecific relationships, on samples of Neopetrosia chaliniformis from various locations in the Indo-Pacific and compare its variation with a mitochondrial marker (CO2). LTRS recovers several reciprocal monophyletic groups among the Indo-Pacific N. chaliniformis and provides a potential alternative to ATPSβ.

Keywords

PoriferaspongesNeopetrosiamarkernuclear DNAintronlysidyl aminoacyl transfer RNA synthetaseLTRS
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 2: Proceedings of the 9th World Sponge Conference held in Fremantle Australia in 2013: New Frontiers in Sponge Science , March 2016 , pp. 333 - 339
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abdillah, S., Nurhayati, A.P.D., Nurhatika, S., Setiawan, E. and Heffen, W.L. (2013 a) Cytotoxic and antioxidant activities of marine sponge diversity at Pecaron Bay Pasir Putih Situbondo East Java, Indonesia. Journal of Pharmacy Research 6, 685–689.CrossRefGoogle Scholar
Abdillah, S., Wahida Ahmad, R., Kamal Muzaki, F. and Mohd Noor, N. (2013 b) Antimalarial activity of Neopetrosia exigua extract in mice. Journal of Pharmacy Research 6, 799–803.CrossRefGoogle Scholar
Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Avise, J.C. (1998) Conservation genetics in the marine realm. Journal of Heredity 89, 377–382.CrossRefGoogle Scholar
Becking, L.E., Erpenbeck, D., Peijnenburg, K.T. and de Voogd, N.J. (2013) Phylogeography of the sponge Suberites diversicolor in Indonesia: insights into the evolution of marine lake populations. PLoS ONE 8, e75996.CrossRefGoogle ScholarPubMed
Bentlage, B. and Wörheide, G. (2007) Low genetic structuring among Pericharax heteroraphis (Porifera: Calcarea) populations from the Great Barrier Reef (Australia), revealed by analysis of rDNA and nuclear intron sequences. Coral Reefs 26, 807–816.CrossRefGoogle Scholar
Clancy, S. (2008) RNA splicing: Introns, exons and spliceosome. Nature Education 1, 31.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.CrossRefGoogle ScholarPubMed
de Almeida Leone, P., Carroll, A.R., Towerzey, L., King, G., McArdle, B.M., Kern, G., Fisher, S., Hooper, J.N.A. and Quinn, R.J. (2008) Exiguaquinol: a novel pentacyclic hydroquinone from Neopetrosia exigua that inhibits Helicobacter pylori MurI. Organic Letters 10, 2585–2588.CrossRefGoogle ScholarPubMed
de Voogd, N.J. and Cleary, D.F.R. (2008) An analysis of sponge diversity and distribution at three taxonomic levels in the Thousand islands/Jakarta bay reef complex, West-Java, Indonesia. Marine Ecology 29, 205–215.CrossRefGoogle Scholar
DeBiasse, M.B., Richards, V.P. and Shivji, M.S. (2010) Genetic assessment of connectivity in the common reef sponge, Callyspongia vaginalis (Demospongiae: Haplosclerida) reveals high population structure along the Florida reef tract. Coral Reefs 29, 47–55.CrossRefGoogle Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Erpenbeck, D., Breeuwer, J.A.J., van der Velde, H.C. and Soest, R.W.M.v. (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Marine Biology 141, 377–386.Google Scholar
Erpenbeck, D., McCormack, G., Breeuwer, J. and van Soest, R. (2004) Order level differences in the structure of partial LSU across demosponges (Porifera): New insights into an old taxon. Molecular Phylogenetics and Evolution 32, 388–395.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolution Bioinformatics Online 1, 47–50.Google Scholar
Flot, J.F. (2010) Seqphase: a web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources 10, 162–166.CrossRefGoogle ScholarPubMed
Hoeksema, B. (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the coral triangle. In Renema, W. (ed.) Biogeography, time, and place: distributions, barriers, and islands. Amsterdam: Springer, pp. 117–178.CrossRefGoogle Scholar
Huang, D., Meier, R., Todd, P. and Chou, L. (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution 66, 167–174.CrossRefGoogle ScholarPubMed
Jarman, S.N., Ward, R.D. and Elliott, N.G. (2002) Oligonucleotide primers for PCR amplification of coelomate introns. Marine Biotechnology 4, 347–355.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lim, S.C., de Voogd, N., Tan, K.S. and Singapore, S.C. (2008) A guide to sponges of Singapore. Singapore: Science Centre Singapore, pp. 1–173.Google Scholar
Lopez-Legentil, S. and Pawlik, J.R. (2009) Genetic structure of the Caribbean giant barrel sponge Xestospongia muta using the I3-M11 partition of COI. Coral Reefs 28, 157–165.CrossRefGoogle Scholar
Maldonado, M. and Uriz, M.J. (1999) Sexual propagation by sponge fragments. Nature 398, 476.CrossRefGoogle Scholar
Moore, W.S. (1995) Inferring phylogenies from mtDNA variation – mitochondrial-gene trees vs nuclear-gene trees. Evolution 49, 718–726.Google Scholar
Orabi, K.Y., El Sayed, K.A., Hamann, M.T., Dunbar, D.C., Al-Said, M.S., Higa, T. and Kelly, M. (2002) Araguspongines K and L, new bioactive Bis-1-oxaquinolizidine N-oxide alkaloids from Red Sea specimens of Xestospongia exigua. Journal of Natural Products 65, 1782–1785.CrossRefGoogle ScholarPubMed
Palumbi, S.R. and Baker, C.S. (1994) Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales. Molecular Biology and Evolution 11, 426–435.Google ScholarPubMed
Reveillaud, J., Remerie, T., van Soest, R., Erpenbeck, D., Cardenas, P., Derycke, S., Xavier, J.R., Rigaux, A. and Vanreusel, A. (2010) Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae). Molecular Phylogenetics and Evolution 56, 104–114.CrossRefGoogle ScholarPubMed
Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle ScholarPubMed
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. and Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rua, C.P.J., Zilberberg, C. and Sole-Cava, A.M. (2011) New polymorphic mitochondrial markers for sponge phylogeography. Journal of the Marine Biological Association of the United Kingdom 91, 1015–1022.CrossRefGoogle Scholar
Sambrook, E., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning. A laboratory manual. New York, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Shearer, T.L., van Oppen, M.J.H., Romano, S.L. and Wörheide, G. (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 2475–2487.CrossRefGoogle ScholarPubMed
Silvestro, D. and Michalak, I. (2012) RaxmlGUI: A graphical front-end for RAxML. Organisms Diversity and Evolution 12, 335–337.CrossRefGoogle Scholar
Stamatakis, A. (2008) The RAxML 7.0.4 manual. http://icwww.epfl.ch/~stamatak/index-DateiencountManual7.0.4.php. Accessed 21 January 2013.Google Scholar
Stamatakis, A., Hoover, P. and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.CrossRefGoogle ScholarPubMed
Swierts, T., Peijnenburg, K.T.C.A., de Leeuw, C., Cleary, D.F.R., Hörnlein, C., Setiawan, E., Wörheide, G., Erpenbeck, D. & de Voogd, N.J. (2013) Lock, stock and two different barrels: comparing the genetic composition of morphotypes of the Indo-Pacific sponge Xestospongia testudinaria. PLoS ONE 8, e74396.CrossRefGoogle ScholarPubMed
Thomas, J.A., Welch, J.J., Woolfit, M. and Bromham, L. (2006) There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. Proceedings of the National Academy of Sciences USA 103, 7366–7371.CrossRefGoogle Scholar
Thomson, R.C., Wang, I.J. and Johnson, J.R. (2010) Genome-enabled development of DNA markers for ecology, evolution and conservation. Molecular Ecology 19, 2184–2195.CrossRefGoogle ScholarPubMed
van Soest, R.W.M. (1989) The Indonesian sponge fauna: a status report. Netherlands Journal of Sea Research 23, 223–230.CrossRefGoogle Scholar
Vargas, S., Schuster, A., Sacher, K., Büttner, G., Schätzle, S., Läuchli, B., Hall, K., Hooper, J.N.A., Erpenbeck, D. and Wörheide, G. (2012) Barcoding sponges: an overview based on comprehensive sampling. PLoS ONE 7, e39345.CrossRefGoogle ScholarPubMed
Wörheide, G., Epp, L. and Macis, L. (2008) Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both? BMC Evolutionary Biology 8, 24.CrossRefGoogle ScholarPubMed
Wörheide, G., Sole-Cava, A.M. and Hooper, J.N.A. (2005) Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks. Integrative and Comparative Biology 45, 377–385.CrossRefGoogle ScholarPubMed
Wares, J.P., Pankey, M.S., Pitombo, F., Gómez Daglio, L. and Achituv, Y. (2009) A “shallow phylogeny” of shallow barnacles (Chthamalus). PLoS ONE 4, e5567.CrossRefGoogle Scholar
Wiens, J.J., Kuczynski, C.A. and Stephens, P.R. (2010) Discordant mitochondrial and nuclear gene phylogenies in emydid turtles: implications for speciation and conservation. Biological Journal of the Linnean Society 99, 445–461.CrossRefGoogle Scholar
Wulff, J.L. (1995) Effects of a hurricane on survival and orientation of large erect coral reef sponges. Coral Reefs 14, 55–61.CrossRefGoogle Scholar
Xavier, J.R., van Soest, R.W.M., Breeuwer, J.A., Martins, A.M. and Menken, S.B. (2010) Phylogeography, genetic diversity and structure of the poecilosclerid sponge Phorbas fictitius at oceanic islands. Contributions to Zoology 79, 119–129.CrossRefGoogle Scholar
Zhang, D.-X. and Hewitt, G.M. (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Molecular Ecology 12, 563–584.CrossRefGoogle ScholarPubMed
Supplementary material: File

Setiawan Supplementary material

Table

Download Setiawan Supplementary material(File)
File 117.8 KB