Hydrobiologia

, Volume 687, Issue 1, pp 61–69

The complete mitochondrial genome of the verongid sponge Aplysina cauliformis: implications for DNA barcoding in demosponges

  • Erik A. Sperling
  • Rafael D. Rosengarten
  • Maria A. Moreno
  • Stephen L. Dellaporta
SPONGE RESEARCH DEVELOPMENTS

Abstract

DNA “barcoding,” the determination of taxon-specific genetic variation typically within a fragment of the mitochondrial cytochrome oxidase 1 (cox1) gene, has emerged as a useful complement to morphological studies, and is routinely used by expert taxonomists to identify cryptic species and by non-experts to better identify samples collected during field surveys. The rate of molecular evolution in the mitochondrial genomes (mtDNA) of nonbilaterian animals (sponges, cnidarians, and placozoans) is much slower than in bilaterian animals for which DNA barcoding strategies were developed. If sequence divergence among nonbilaterian mtDNA and specifically cox1 is too slow to generate diagnostic variation, alternative genes for DNA barcoding and species-level phylogenies should be considered. Previous study across the Aplysinidae (Demospongiae, Verongida) family of sponges demonstrated no nucleotide substitutions in the traditional cox1 barcoding fragment among the Caribbean species of Aplysina. As the mitochondrial genome of Aplysina fulva has previously been sequenced, we are now able to make the first comparisons between complete mtDNA of congeneric demosponges to assess whether potentially informative variation exists in genes other than cox1. In this article, we present the complete mitochondrial genome of Aplysina cauliformis, a circular molecule 19620 bp in size. The mitochondrial genome of A. cauliformis is the same length as is A. fulva and shows six confirmed nucleotide differences and an additional 11 potential SNPs. Of the six confirmed SNPs, NADH dehydrogenase subunit 5 (nad5) and nad2 each contain two, and in nad2 both yield amino acid substitutions, suggesting balancing selection may act on this gene. Thus, while the low nucleotide diversity in Caribbean aplysinid cox1 extends to the entire mitochondrial genome, some genes do display variation. If these represent interspecific differences, then they may be useful alternative markers for studies in recently diverged sponge clades.

Keywords

mtDNA Porifera Demospongiae Verongida 

Abbreviations

mtDNA

Mitochondrial genome

atp6, 8, 9

ATP synthase F0 subunit #

cob

Apocytochrome b

cox1-3

Cytochrome c oxidase #

nad1-6, 4L

NADH dehydrogenase subunit #

rnS

Small ribosomal RNA

rnL

Large ribosomal RNA

Supplementary material

10750_2011_879_MOESM1_ESM.pdf (2.9 mb)
Supplementary material 1 (PDF 2991 kb)
10750_2011_879_MOESM2_ESM.jpg (356 kb)
Supplementary material 2 (JPG 356 kb)
10750_2011_879_MOESM3_ESM.doc (26 kb)
Supplementary material 3 (DOC 26 kb)

References

  1. Bell, J. J., 2008. The functional roles of marine sponges. Estuarine, Coastal and Shelf Sciences 79: 341–353.CrossRefGoogle Scholar
  2. Blanquer, A. & M.-J. Uriz, 2007. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Molecular Phylogenetics and Evolution 45: 392–397.PubMedCrossRefGoogle Scholar
  3. Boore, J. L. & W. M. Brown, 1998. Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Current Opinions in Genetics and Development 8: 668–674.CrossRefGoogle Scholar
  4. Borchiellini, C., C. Chombard, M. Manuel, E. Alivon, J. Vacelet & N. Boury-Esnault, 2004. Molecular phylogeny of Demospongiae: implications for classifications and scenarios of character evolution. Molecular Phylogenetics and Evolution 32: 823–837.PubMedCrossRefGoogle Scholar
  5. Chen, J. & S. L. Dellaporta, 1994. Urea-based plant DNA miniprep. In Freeling, M. & V. Walbot (eds), The maize handbook. Springer, New York: 526–527.Google Scholar
  6. Drabkin, H. J., M. Estrella & U. L. Rajbhandary, 1998. Initiator-elongator discrimination in vertebrate tRNAs for protein synthesis. Molecular and Cellular Biology 18: 1459–1466.PubMedGoogle Scholar
  7. Duran, S., M. Pascual & X. Turon, 2004. Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Marine Biology 144: 31–35.CrossRefGoogle Scholar
  8. Erpenbeck, D., J. N. A. Hooper & G. Wörheide, 2005. CO1 phylogenies in diploblasts and the ‘Barcoding of Life’—are we sequencing a suboptimal partition? Molecular Ecology Notes 6: 550–553.CrossRefGoogle Scholar
  9. Erwin, P. M. & R. W. Thacker, 2007. Phylogenetic analysis of marine sponges within the order Verongida: a comparison of morphological and molecular data. Invertebrate Biology 126: 220–234.CrossRefGoogle Scholar
  10. Ewing, B. & P. Green, 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8: 186–194.PubMedGoogle Scholar
  11. Folmer, O., M. Black, W. Hoen, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.PubMedGoogle Scholar
  12. Galtier, N., B. Nabholz, S. Glemin & G. D. D. Hurst, 2009. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18: 4541–4550.PubMedCrossRefGoogle Scholar
  13. Gordon, D., C. Abajian & P. Green, 1998. Consed: a graphical tool for sequence finishing. Genome Research 8: 195–202.PubMedGoogle Scholar
  14. Haag-Liautard, C., N. Coffey, D. Houle, M. Lynch, B. Charlesworth & P. D. Keightley, 2008. Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biology 6(8): e204.PubMedCrossRefGoogle Scholar
  15. Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. Dewaard, 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society London B 270: 313–321.CrossRefGoogle Scholar
  16. Heim, I., M. Nickel & F. Brummer, 2007a. Phylogeny of the genus Tethya (Tethyidae: Hadromerida: Porifera): molecular and morphological aspects. Journal of the Marine Biological Association of the United Kingdom 87: 1615–1627.CrossRefGoogle Scholar
  17. Heim, I., N. Nickel & F. Brummer, 2007b. Molecular markers for species discrimination in poriferans: a case study on species of the genus Aplysina. Porifera Research 1: 361–371.Google Scholar
  18. Huang, D., R. Meier, P. A. Todd & L. M. Chou, 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.PubMedCrossRefGoogle Scholar
  19. Klautau, M., C. A. M. Russo, C. Lazoski, N. Boury-Esnault, J. P. Thorpe & A. M. Sole-Cava, 1999. Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53:1414–1422.Google Scholar
  20. Kloppell, A., A. Putz, M. Pfannkuchen, G. Fritz, A. Jaklin, P. Proksch & F. Brummer, 2009. Depth profile of Aplysina ssp.: morphological, histological and biochemical aspects and their role in species distinction. Marine Biodiversity 39: 121–129.CrossRefGoogle Scholar
  21. Krzywinski, M., J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S. J. Jones & M. A. Marra, 2009. Circos: an information aesthetic for comparative genomics. Genome Research 19: 1639–1645.PubMedCrossRefGoogle Scholar
  22. Lamarao, F. R. M., E. C. Reis, T. A. Simao, R. M. Albano & G. Lobo-Hadju, 2010. Aplysina (Porifera: Demospongiae) species identification through SSCP-ITS patterns. Journal of the Marine Biological Association of the United Kingdom 90: 845–850.CrossRefGoogle Scholar
  23. Lavrov, D. V., 2007. Key transitions in animal evolution: a mitochondrial DNA perspective. Integrative and Comparative Biology 47: 734–743.PubMedCrossRefGoogle Scholar
  24. Lavrov, D. V., W. M. Brown & J. L. Boore, 2000. A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proceedings of the National Academy of Sciences of the USA 97: 13738–13742.PubMedCrossRefGoogle Scholar
  25. Lavrov, D. V., L. Forget, M. Kelly & B. F. Lang, 2005. Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution. Molecular Biology and Evolution 22: 1231–1239.PubMedCrossRefGoogle Scholar
  26. Lavrov, D. V., X. Wang & M. Kelly, 2008. Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data. Molecular Phylogenetics and Evolution 49: 111–124.PubMedCrossRefGoogle Scholar
  27. Lis, J. T. & R. Schleif, 1975. Size fractionation of double-stranded DNA by precipitation with polyethylene glycol. Nucleic Acids Research 2: 383–389.PubMedCrossRefGoogle Scholar
  28. Lowe, T. M. & S. R. Eddy, 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25: 955–964.PubMedCrossRefGoogle Scholar
  29. Maldonado, M., M. C. Carmona, M. J. Uriz & A. Cruzado, 1999. Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401: 785–788.CrossRefGoogle Scholar
  30. Miller, S. E., 2007. DNA barcoding and the renaissance of taxonomy. Proceedings of the National Academy of Sciences of the USA 12: 4775–4776.CrossRefGoogle Scholar
  31. Muramatsu, T., K. Nishikawa, F. Nemoto, Y. Kuchino, S. Nishimura, T. Miyazawa & S. Yokoyama, 1998. Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature 336: 179–181.CrossRefGoogle Scholar
  32. Nichols, S. A., 2005. An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution 34: 81–96.PubMedCrossRefGoogle Scholar
  33. Pöppe, J., P. Sutcliffe, J. N. A. Hooper, G. Wörheide & D. Erpenbeck, 2010. COI barcoding reveals new clades and radiation patterns of Indo-Pacific sponges of the family Irciniidae (Demospongiae: Dictyoceratida). PloS One 5: e9950.PubMedCrossRefGoogle Scholar
  34. Rosengarten, R. D., E. A. Sperling, M. A. Moreno, S. P. Leys & S. L. Dellaporta, 2008. The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: evidence for programmed translational frameshifting. BMC Genomics 9: 33.PubMedCrossRefGoogle Scholar
  35. Schander, C. & E. Willassen, 2005. What can biological barcoding do for marine biology? Marine Biology Research 1: 79–83.CrossRefGoogle Scholar
  36. Schmitt, S., U. Hentschel, S. Zea, T. Dandekar & M. Wolf, 2005. ITS-2 and 18S rRNA gene phylogeny of Aplysinidae (Verongida, Demospongiae). Journal of Molecular Evolution 60: 327–336.PubMedCrossRefGoogle Scholar
  37. Schroder, H. C., S. M. Efremova, V. B. Itskovich, S. Belikov, Y. Masuda, A. Krasko, I. M. Muller & W. E. G. Muller, 2003. Molecular phylogeny of the freshwater sponges in Lake Baikal. Journal of Zoological Systematics and Evolutionary Research 41: 80–86.CrossRefGoogle Scholar
  38. Shearer, T. L., M. J. H. Van Oppen, S. L. Romano & G. Wörheide, 2002. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11: 2475–2487.PubMedCrossRefGoogle Scholar
  39. Sipkema, D., M. C. R. Franssen, R. Osinga, J. Tramper & R. H. Wijffels, 2005. Marine sponges as pharmacy. Marine Biotechnology 7: 142–162.PubMedCrossRefGoogle Scholar
  40. Sperling, E. A., K. J. Peterson & D. Pisani, 2007. Poriferan paraphyly and its implications for Precambrian palaeobiology. Geological Society, London, Special Publications 286: 355–368.CrossRefGoogle Scholar
  41. Sperling, E. A., K. J. Peterson & D. Pisani, 2009. Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Molecular Biology and Evolution 26: 2261–2274.PubMedCrossRefGoogle Scholar
  42. Stortchevoi, A., U. Varshney & U. L. Rajbhandary, 2003. Common location of determinants in initiator transfer RNAs for initiator-elongator discrimination in bacteria and in eukaryotes. Journal of Biological Chemistry 278: 17672–17679.PubMedCrossRefGoogle Scholar
  43. Tatusova, T. A. & T. L. Madden, 1999. BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiology Letters 174: 247–250.PubMedCrossRefGoogle Scholar
  44. Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.PubMedCrossRefGoogle Scholar
  45. Wang, X. & D. V. Lavrov, 2008. Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PloS One 3: e2723.PubMedCrossRefGoogle Scholar
  46. Weber, F., A. Dietrich, J. H. Weil & L. Marechal-Drouard, 1990. A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucleic Acids Research 18: 5027–5030.PubMedCrossRefGoogle Scholar
  47. Wörheide, G., 2006. Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Marine Biology 148: 907–912.CrossRefGoogle Scholar
  48. Wörheide, G. & D. Erpenbeck, 2007. DNA taxonomy of sponges—progress and perspectives. Journal of the Marine Biological Association of the United Kingdom 87: 1629–1633.CrossRefGoogle Scholar
  49. Wyman, S. K., R. K. Jansen & J. L. Boore, 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252–3255.PubMedCrossRefGoogle Scholar
  50. Xavier, J. R., P. G. Rachello-Dolmen, F. Parra-VElandia, C. H. L. Schonberg, J. A. J. Breeuwer & R. W. M. van Soest, 2010. Molecular evidence of cryptic speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae). Molecular Phylogenetics and Evolution 56: 13–20.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Erik A. Sperling
    • 1
    • 3
  • Rafael D. Rosengarten
    • 2
    • 4
  • Maria A. Moreno
    • 2
  • Stephen L. Dellaporta
    • 2
  1. 1.Department of Geology and GeophysicsYale UniversityNew HavenUSA
  2. 2.Department of Molecular, Cellular and Developmental BiologyYale UniversityNew HavenUSA
  3. 3.Department of Earth and Planetary SciencesHarvard UniversityCambridgeUSA
  4. 4.Lawrence Berkeley National LaboratoryJoint BioEnergy InstituteEmeryvilleUSA

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