Skip to main content

First insights into the phylogeny of deep-sea glass sponges (Hexactinellida) from polymetallic nodule fields in the Clarion-Clipperton Fracture Zone (CCFZ), northeastern Pacific

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

An Opinion Paper to this article was published on 01 August 2018

Abstract

Glass sponges represent a dominant group of megabenthic deep-sea fauna and play a key role in benthic deep-sea ecosystems. Especially in the Clarion-Clipperton Fracture Zone (CCFZ), a potential deep-sea mining area, they grow on polymetallic nodules or on the surrounding sediment. We investigate hexactinellids from the CCFZ to understand the ecological aspects of deep-sea mining and support the development of future pre-mining risk assessments and monitoring actions. Therefore, this study is published as part of a series of studies, all focusing on deep-sea glass sponges from the CCFZ. Resolving genetic relationships between species is still a fundamental as well as challenging task. Especially understudied groups mostly lack resolution. Combining results derived from taxonomic and phylogenetic data gives deeper insights into glass sponge relationships. Here, we present (1) a set of new primers for sequencing mitochondrial 16S rDNA as well as nuclear 18S and 28S rDNA of glass sponges, (2) first DNA sequencing data for 6 hexactinellid genera and 19 species, as well as (3) the most comprehensive phylogenetic tree of hexactinellid sponges to date including data available from previous studies.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Amon, D., A. F. Ziegler, T. G. Dahlgren, A. G. Glover, A. Goineau, A. J. Gooday, H. Wiklund & C. R. Smith, 2016. Insights into the abundance an diversity of abyssal megafauna in a polymetallic-nodule region in the eastern Calrion-Clipperton Zone. Scientific Reports 6: 1–12. https://doi.org/10.1038/srep30492.

    Article  CAS  Google Scholar 

  2. Beaulieu, S. E., 2001. Life on glass houses: sponge stalk communities in the deep sea. Marine Biology 138: 803–817. https://doi.org/10.1007/s002270000500.

    Article  Google Scholar 

  3. Bell, J. J., 2008. The functional roles of marine sponges. Estuarine, Coastal and Shelf Science 79: 341–353. https://doi.org/10.1016/j.ecss.2008.05.002.

    Article  Google Scholar 

  4. Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C. H. Wu, D. Xie, M. A. Suchard, A. Rambaut & A. J. Drummond, 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10: e1003537. https://doi.org/10.1371/journal.pcbi.1003537.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Collins, A. G., 1998. Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proceedings of the National Academy of Sciences of the United States of America 95: 15458–15463. PMCID:PMC28064

  6. Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Dohrmann, M., D. Janussen, J. Reitner, A. G. Collins & G. Wörheide, 2008. Phylogeny and evolution of glass sponges (Porifera, Hexactinellida). Systematic Biology 57: 388–405. https://doi.org/10.1080/10635150802161088.

    Article  PubMed  CAS  Google Scholar 

  8. Dohrmann, M., A. G. Collins & G. Wörheide, 2009. New insights into the phylogeny of glass sponges (Porifera, Hexactinellida): monophyly of Lyssacinosida and Euplectellinae and the phylogenetic position of Euretidae. Molecular Phylogenetics and Evolution 52: 257–262. https://doi.org/10.1016/j.ympev.2009.01.010.

    Article  PubMed  CAS  Google Scholar 

  9. Dohrmann, M., K. M. Haen, D. V. Lavrov & G. Wörheide, 2011. Molecular phylogeny of glass sponges (Porifera, Hexactinellida): increased taxon sampling and inclusion of the mitochondrial protein-coding gene, cytochrome oxidase subunit I. Hydrobiologia 687: 11–20. https://doi.org/10.1007/s10750-011-0727-z.

    Article  CAS  Google Scholar 

  10. Dohrmann, M., C. Göcke, J. Reed & D. Janussen, 2012. Integrative taxonomy justifies a new genus, Nodastrella gen. nov., for North Atlantic “Rossella” species (Porifera: Hexactinellida: Rossellidae). Zootaxa 3383: 1–13. https://doi.org/10.11646/zootaxa.3383.1.1.

    Article  Google Scholar 

  11. Gollner, S., S. Kaiser, L. Menzel, D. O. B. Jones, A. Brown, N. C. Mestre, D. Van Oevelen, L. Menot, A. Colaço, M. Canals, D. Cuvelier, J. M. Durden, A. Gebruk, G. A. Egho, M. Haeckel, Y. Marcon, L. Mevenkamp, T. Morato, C. K. Pham, A. Purser, A. Sanchez-Vidal, A. Vanreusel, A. Vink & P. Martínez Arbizu, 2017. Resilience to benthic deep-sea fauna to mining activities. Marine Environmental Research. https://doi.org/10.1016/j.marenvres.2017.04.010.

    PubMed  Article  Google Scholar 

  12. Gong, L., L. Xinzheng & Q. Jian-Wen, 2015. Two new species of Hexactinellida (Porifera) from the South China Sea. Zootaxa 4034: 182–192.

    Article  PubMed  Google Scholar 

  13. Guindon, S. & O. Gascuel, 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52: 696–704.

    Article  PubMed  Google Scholar 

  14. Haen, K. M., W. Pett & D. V. Lavrov, 2013. Eight new mtDNA sequences of glass sponges reveal an extensive usage of + 1 frameshifting in mitochondrial translation. Gene 535: 336–344.

    Article  PubMed  CAS  Google Scholar 

  15. Higgins, D., J. Thompson, T. Gibson, J. D. Thompson, 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.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hogg, M. M., O. S. Tendal, K. W. Conway, S. A. Pomponi, R. W. M. Van Soest, J. Gutt, M. Krautter & J. M. Roberts, 2010. Deep-sea sponge grounds: reservoirs of biodiversity. UNEP-WCMC Biodiversity Series 32. UNEP-WCMC, Cambridge, UK.

  17. Ivanova, N., J. deWaard & P. Hebert, 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6: 998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x.

    Article  CAS  Google Scholar 

  18. Kahn, A. S., J. B. Geller, H. M. Reiswig & K. L. Smith Jr., 2013. Bathydorus laniger and Docosaccus maculatus (Lyssacinosida; Hexactinellida): two new species of glass sponge from the abyssal eastern North Pacific Ocean. Zootaxa 3646: 386–400.

    Article  PubMed  Google Scholar 

  19. Kaiser, S., C. R. Smith & P. Martínez Arbizu, 2017. Editorial: biodiversity of the Clarion Clipperton Fracture Zone. Marine Biodiversity. https://doi.org/10.1007/s12526-017-0733-0.

    Article  Google Scholar 

  20. Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Meintjes & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Kersken, D., D. Janussen & P. Martínez Arbizu, 2017. Deep-sea glass sponges (Hexactinellida) from polymetallic nodule fields in the Clarion-Clipperton Fracture Zone (CCFZ), northeastern Pacific: part I – Amphidiscophora. Marine Biodiversity. https://doi.org/10.1007/s12526-017-0727-y.

    Article  Google Scholar 

  22. Kersken, D., D. Janussen & P. Martínez Arbizu, 2018. Deep-sea glass sponges (Hexactinellida) from polymetallic nodule fields in the Clarion-Clipperton Fracture Zone (CCFZ), northeastern Pacific: Part II – Hexasterophora. Marine Biodiversity (submitted).

  23. Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology Evolution 33: 1870–1874.

    Article  PubMed  CAS  Google Scholar 

  24. Petersen, S., A. Krätschell, N. Augustin, J. Jamieson, J. R. Hein & M. D. Hannington, 2016. News from the seabed – geological characteristics and resource potential of deep-sea mineral resources. Marine Policy 70: 175–187. https://doi.org/10.1016/j.marpol.2016.03.012.

    Article  Google Scholar 

  25. Purser, A., Y. Marcon, H. J. T. Hoving, M. Vecchione, U. Piatkowski, D. Eason, H. Bluhm & A. Boetius, 2016. Association of deep-sea incirrate octopods with manganese crusts and nodule fields in the Pacific Ocean. Current Biology 26: R1268–R1269.

    Article  PubMed  CAS  Google Scholar 

  26. Rambaut, A., 2016. FigTree v1.4.3 [available on internet at http://tree.bio.ed.ac.uk/software/figtree/].

  27. Rambaut, A., M. A. Suchard, D. Xie & A. J. Drummond, 2014. Tracer v1.6 [available on internet at http://beast.bio.ed.ac.uk/Tracer].

  28. Reiswig, H. M. & M. Dohrmann, 2014. Three new species of glass sponges (Porifera: Hexactinellida) from the West Indies, and molecular phylogenetics of Euretidae and Auloplacidae (Sceptrulophora). Zoological Journal of the Linnean Society 171: 233–253.

    Article  Google Scholar 

  29. Tavare, S., 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. American Mathematical Society: Lectures on Mathematics in the Life Sciences 17: 57–86.

    Google Scholar 

  30. Thiel, H., 2001. Evaluation of the environmental consequences of polymetallic nodule mining based on the results of the TUSCH research association. Deep-Sea Research II 48: 3433–3452.

    Article  CAS  Google Scholar 

  31. Truett, G. E., P. Heeger, R. L. Mynatt, A. A. Truett, J. A. Walker & M. L. Warman, 2000. Preparation of PCR quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques 29: 52–54.

    PubMed  CAS  Article  Google Scholar 

  32. Vanreusel, A., A. Hialrio, P. A. Ribeiro, L. Menot & P. Martínez Arbizu, 2016. Threatened by mining, polymetallic nodules are required to preserve abyssal fauna. Nature – Scientific Reports 6: 26808. https://doi.org/10.1038/srep26808

  33. Van Soest, R. V. M., N. Boury-Esnault, J. Vacelet, M. Dohrmann, D. Erpenbeck, N. J. De Voogd, N. Santodomingo, B. Vanhoorne, M. Kelly & J. N. A. Hooper, 2012. Global diversity of sponges (Porifera). PLoS One 7: e35105.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Vargas, S., M. Dohrmann, C. Göcke, D. Janussen & G. Wörheide, 2017. Nuclear and mitochondrial phylogeny of Rossella (Hexactinellida: Lyssacinosida, Rossellidae): a species and a species flock in the Southern Ocean. Polar Biology. https://doi.org/10.1007/s00300-017-2155-7.

    Article  Google Scholar 

  35. Wedding, L. M., S. M. Reiter, C. R. Smith, K. M. Gjerde, J. M. Kittinger, A. M. Friedlander, S. D. Gaines, M. R. Clark, A. M. Thurnherr, S. M. Hardy & L. B. Crowder, 2015. Managing mining of the deep seabed. Science 349: 144–145.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The EcoResponse cruise with RV Sonne was financed by the German Ministry of Education and Science (BMBF) as a contribution to the European project JPI-Oceans “Ecological Aspects of Deep-Sea Mining”. The authors acknowledge funding from BMBF under Contract 03F0707E. Furthermore, we want to thank Dr. Barbara Feldmeyer and Dr. Ann-Marie Waldvogel for assistance of molecular lab work and Dr. Martin Dohrmann for information on sponge specific DNA primers and PCR protocols.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daniel Kersken.

Additional information

GenBank: All nucleotide sequences used in this study have accession numbers at GenBank (https://www.ncbi.nlm.nih.gov/genbank/) (Supplementary Material 3).

Handling editor: Iacopo Bertocci

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kersken, D., Kocot, K., Janussen, D. et al. First insights into the phylogeny of deep-sea glass sponges (Hexactinellida) from polymetallic nodule fields in the Clarion-Clipperton Fracture Zone (CCFZ), northeastern Pacific. Hydrobiologia 811, 283–293 (2018). https://doi.org/10.1007/s10750-017-3498-3

Download citation

Keywords

  • Sponge phylogeny
  • DNA barcoding
  • Manganese nodules
  • Deep-sea mining