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.
Similar content being viewed by others
References
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.
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.
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.
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.
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
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.
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.
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.
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.
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.
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.
Gong, L., L. Xinzheng & Q. Jian-Wen, 2015. Two new species of Hexactinellida (Porifera) from the South China Sea. Zootaxa 4034: 182–192.
Guindon, S. & O. Gascuel, 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52: 696–704.
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.
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.
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.
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.
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.
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.
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.
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.
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).
Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology Evolution 33: 1870–1874.
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.
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.
Rambaut, A., 2016. FigTree v1.4.3 [available on internet at http://tree.bio.ed.ac.uk/software/figtree/].
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].
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.
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.
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.
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.
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
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.
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.
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.
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
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Iacopo Bertocci
GenBank: All nucleotide sequences used in this study have accession numbers at GenBank (https://www.ncbi.nlm.nih.gov/genbank/) (Supplementary Material 3).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-017-3498-3