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A Mitochondrial Intron in a Verongid Sponge

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Abstract

We discovered for the first time a mitochondrial intron in a non-tetillid demosponge, which sheds new light on the interpretation of mitochondrial intron evolution among non-bilaterian animals and has consequences for phylogenetic and DNA barcoding studies. The newly discovered class 1 intron of Aplysinella rhax (Verongida) CO1 has an ORF for a putative LAGLIDADG-type and resembles other sponge and cnidarian mitochondrial introns. Our analysis of the Aplysinella rhax intron underlines that the patchy distribution of introns in sponges is caused by a combination of horizontal and vertical transmission. Further implications for CO1 phylogenetic and barcoding projects are discussed.

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References

  • Beagley CT, Okada NA, Wolstenholme DR (1996) Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc Natl Acad Sci USA 93:5619–5623

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Burger G, Forget L, Zhu Y, Gray MW, Lang BF (2003) Unique mitochondrial genome architecture in unicellular relatives of animals. Proc Natl Acad Sci USA 100:892–897

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Burt A, Koufopanou V (2004) Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr Opin Genet Dev 14:609–615

    Article  CAS  PubMed  Google Scholar 

  • Cho S, Jin SW, Cohen A, Ellis RE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14:1207–1220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Laubenfels MW (1954) The sponges of the West-Central Pacific. Oregon State monographs. Studies in zoology, no. 7, pp i–x, 1–306, I–XII

  • Dellaporta SL, Xu A, Sagasser S, Jakob W, Moreno MA, Buss LW, Schierwater B (2006) Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum. Proc Natl Acad Sci USA 103:8751–8756

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Edgell DR (2009) Selfish DNA: homing endonucleases find a home. Curr Biol 19:R115–R117

    Article  CAS  PubMed  Google Scholar 

  • Erpenbeck D, Duran S, Rützler K, Paul V, Hooper JNA, Wörheide G (2007) Towards a DNA taxonomy of Caribbean demosponges: a gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae. J Mar Biol Soc U. K. 87:1563–1570

    CAS  Google Scholar 

  • Erpenbeck D, Voigt O, Wörheide G, Lavrov DV (2009) The mitochondrial genomes of sponges provide evidence for multiple invasions by Repetitive Hairpin-forming Elements (RHE). BMC Genom 10:591

    Article  Google Scholar 

  • Erpenbeck D, Sutcliffe P, Cook SdC, Dietzel A, Maldonado M, van RWM Soest, Hooper JNA, Wörheide G (2012) Horny sponges and their affairs: on the phylogenetic relationships of keratose sponges. Mol Phylogenet Evol 63:809–816

    Article  PubMed  Google Scholar 

  • Fukami H, Chen CA, Chiou CY, Knowlton N (2007) Novel group I introns encoding a putative homing endonuclease in the mitochondrial cox1 gene of Scleractinian corals. J Mol Evol 64:591–600

    Article  CAS  PubMed  Google Scholar 

  • Gazave E, Lapébie P, Renard E, Vacelet J, Rocher C, Ereskovsky AV, Lavrov DV, Borchiellini C (2010) Molecular phylogeny restores the supra-generic subdivision of homoscleromorph sponges (Porifera, Homoscleromorpha). PLoS One 5(12):e14290

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haugen P, Simon DM, Bhattacharya D (2005) The natural history of group I introns. Trends Genet 21:111–119

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lavrov DV, Forget L, Kelly M, Lang BF (2005) Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution. Mol Biol Evol 22:1231–1239

    Article  CAS  PubMed  Google Scholar 

  • Lavrov D, Pett W, Voigt O, Wörheide G, Forget L, Lang BF, Kayal E (2013) Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): six linear chromosomes, fragmented rRNAs, tRNA editing, and a novel genetic code. Mol Biol Evol 30:865–880

    Article  CAS  PubMed  Google Scholar 

  • Maddison DR, Baker MD, Ober KA (1999) Phylogeny of carabid beetles as inferred from 18S ribosomal DNA (Coleoptera : Carabidae). Syst Entomol 24:103–138

    Article  Google Scholar 

  • Miyamoto M (1999) Molecular systematics: perfect SINEs of evolutionary history? Curr Biol 9:R816–R819

    Article  CAS  PubMed  Google Scholar 

  • Pett W, Ryan J, Pang K, Mullikin J, Martindale M, Baxevanis A, Lavrov D (2011) Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: insight from mtDNA and the nuclear genome. Mitochondrial DNA 22:130–142

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Redmond NE, Morrow CC, Thacker RW, Díaz MC, Boury-Esnault N, Cárdenas P, Hajdu E, Lobo-Hajdu G, Picton BE, Pomponi SA, Kayal E, Collins AG (2013) Phylogeny and systematics of Demospongiae in light of new small-subunit ribosomal DNA (18S) sequences. Integr Comp Biol 53:388–415

    Article  CAS  PubMed  Google Scholar 

  • Rot C, Goldfarb I, Ilan M, Huchon D (2006) Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evol Biol 6:71

    Article  PubMed Central  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Szitenberg A, Rot C, Ilan M, Huchon D (2010) Diversity of sponge mitochondrial introns revealed by cox 1 sequences of Tetillidae. BMC Evol Biol 10:288

    Article  PubMed Central  PubMed  Google Scholar 

  • Uliczka E. (1929) Die tetraxonen Schwämme Westindiens (auf Grund der Ergebnisse der Reise Kükenthal-Hartmeyer). In: Kükenthal W, Hartmeyer R (eds) Ergebnisse einer zoologischen Forschungsreise nach Westindien. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Thiere, Supplement 16, pp 35–62

  • Vacelet J, Bitar G, Carteron S, Zibrowius H, Perez T (2007) Five new sponge species (Porifera: Demospongiae) of subtropical or tropical affinities from the coast of Lebanon (eastern Mediterranean). J Mar Biol Assoc UK 87(6):1539–1552

  • Vallès Y, Halanych KM, Boore JL (2008) Group II introns break new boundaries: presence in a bilaterian’s genome. PLoS One 3:e1488

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, De Voogd NJ, Santodomingo N, Vanhoorne B, Kelly M, Hooper JNA (2012) Global diversity of sponges (Porifera). PLoS One 7:e35105

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang X, Lavrov D (2008) Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS One 3:e2723

    Article  PubMed Central  PubMed  Google Scholar 

  • Wörheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C, Lavrov D (2012) Deep phylogeny and evolution of sponges (Phylum Porifera). Adv Mar Biol 61:1–78

    Article  PubMed  Google Scholar 

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Acknowledgements

DE and GW thank the Deutsche Forschschungsgemeinschaft (DFG) for financial support (Er611/3-1, Wo896/15-1) and acknowledge funding through the LMU Munich’s Institutional Strategy LMUexcellent (Project MODELSPONGE) within the framework of the German Excellence Initiative.

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The authors declare that they have no conflict of interest.

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Correspondence to Dirk Erpenbeck.

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Erpenbeck, D., Aryasari, R., Hooper, J.N.A. et al. A Mitochondrial Intron in a Verongid Sponge. J Mol Evol 80, 13–17 (2015). https://doi.org/10.1007/s00239-014-9653-9

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  • DOI: https://doi.org/10.1007/s00239-014-9653-9

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