The Porifera Ontology (PORO): enhancing sponge systematics with an anatomy ontology

Journal of Biomedical Semantics

Christopher J Mungall¹  Melissa A Haendel²  Erik Segerdell²  Régine Vignes-Lebbe⁴  Adeline Kerner⁴  Maria Cristina Díaz³  Robert W Thacker⁵ 

[1] Genomics Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA;Department of Medical Informatics and Clinical Epidemiology, Oregon Health & Science University, Portland, USA;Museo Margarita, Boca de Rio 6304, Venezuela;CR2P, UMR 7207 CNRS-MNHN-UPMC, Département Histoire de la Terre, Muséum National d’Histoire Naturelle, Bâtiment de Géologie, CP48, 57 rue Cuvier, 75005 Paris, France;Department of Biology, University of Alabama at Birmingham, Birmingham, USA

关键词: Evolution;    Phylogenetics;    Taxonomic identification;    Morphology;   

Others  :  1133545
DOI  :  10.1186/2041-1480-5-39

 received in 2013-07-01, accepted in 2014-07-22,  发布年份 2014

【 摘 要 】

Background

Porifera (sponges) are ancient basal metazoans that lack organs. They provide insight into key evolutionary transitions, such as the emergence of multicellularity and the nervous system. In addition, their ability to synthesize unusual compounds offers potential biotechnical applications. However, much of the knowledge of these organisms has not previously been codified in a machine-readable way using modern web standards.

Results

The Porifera Ontology is intended as a standardized coding system for sponge anatomical features currently used in systematics. The ontology is available from http://purl.obolibrary.org/obo/poro.owl webcite, or from the project homepage http://porifera-ontology.googlecode.com/ webcite. The version referred to in this manuscript is permanently available from http://purl.obolibrary.org/obo/poro/releases/2014-03-06/ webcite.

Conclusions

By standardizing character representations, we hope to facilitate more rapid description and identification of sponge taxa, to allow integration with other evolutionary database systems, and to perform character mapping across the major clades of sponges to better understand the evolution of morphological features. Future applications of the ontology will focus on creating (1) ontology-based species descriptions; (2) taxonomic keys that use the nested terms of the ontology to more quickly facilitate species identifications; and (3) methods to map anatomical characters onto molecular phylogenies of sponges. In addition to modern taxa, the ontology is being extended to include features of fossil taxa.

【 授权许可】

   
2014 Thacker et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Hooper JNA, Van Soest RWM: Systema Porifera. A Guide to the Classification of Sponges. New York: Kluwer Academic; 2002.
• [2]Boury-Esnault N, Rützler K: Thesaurus of Sponge Morphology. Washington: Smithsonian Institution Press; 1997.
• [3]Bergquist P: Sponges. Berkeley: University of California Press; 1978.
• [4]Domingo M: A prototype expert system involved in classificatory tasks for sponge identification. Sci Mar 1993, 57:273-282.
• [5]Domingo M, Godo L, Sierra C: Handling Imperfect Knowledge in Milord II for the Identification of Marine Sponges. In Applications of Uncertainty Formalisms. Edited by Hunter A, Parsons S. Berlin: Springer; 1998:88-137.
• [6]Van Soest RWM, Schalk PH, Smith K, Picton BE, Brugman M, Díaz MC, Sanders ML, De Weerdt WH, Rützler K: POR-LINNAEUS: The application of interactive multimedia software for species data storage and computer assisted identification of Porifera. Bull Kon Belg Inst Natuurwet Biol 1996, 66:63-72.
• [7]Slattery M, Lesser MP, Brazeau D, Stokes MD, Leichter JJ: Connectivity and stability of mesophotic coral reefs. J Exp Mar Bio Ecol 2011, 408:32-41.
• [8]Freeman CJ, Thacker RW: Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr 2011, 56:1577-1586.
• [9]Díaz MC, Rützler K: Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 2001, 69:535-546.
• [10]Leal MC, Puga J, Serôdio J, Gomes NCM, Calado R: Trends in the discovery of new marine natural products from invertebrates over the last two decades–where and what are we bioprospecting? PLoS One 2012, 7:e30580.
• [11]Nichols SA, Roberts BW, Richter DJ, Fairclough SR, King N: Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β-catenin complex. Proc Natl Acad Sci U S A 2012, 109:13046-13051.
• [12]Leys SP, Hill A: The physiology and molecular biology of sponge tissues. Adv Mar Biol 2012, 62:1-56.
• [13]Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang I-F, Tidor B, Degnan BM, Oakley TH, Kosik KS: A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2007, 2:e506.
• [14]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: tool for the unification of biology. Nat Genet 2000, 25:25-29.
• [15]Washington N, Lewis S: Ontologies: Scientific data sharing made easy. Nat Educ 2008, 1:5.
• [16]Hoehndorf R, Dumontier M, Gkoutos GV: Evaluation of research in biomedical ontologies. Brief Bioinform 2012, 14:696-712.
• [17]Bard JBL, Rhee SY: Ontologies in biology: design, applications and future challenges. Nat Rev Genet 2004, 5:213-222.
• [18]Mabee P, Balhoff JP, Dahdul WM, Lapp H, Midford PE, Vision TJ, Westerfield M: 500,000 fish phenotypes: the new informatics landscape for evolutionary and developmental biology of the vertebrate skeleton. J Appl Ichthyol 2012, 28:300-305.
• [19]Mabee PM, Ashburner M, Cronk Q, Gkoutos GV, Haendel M, Segerdell E, Mungall CJ, Westerfield M: Phenotype ontologies: the bridge between genomics and evolution. Trends Ecol Evol 2007, 22:345-350.
• [20]Deans AR, Yoder MJ, Balhoff JP: Time to change how we describe biodiversity. Trends Ecol Evol 2012, 27:78-84.
• [21]Horridge M, Drummond N, Goodwin J, Rector A, Stevens R, Wan H: The Manchester OWL Syntax. OWLED 2006. [http://www.webont.org/owled/2006/acceptedLong/submission_9.pdf webcite]
• [22]Smith B, Ashburner M, Rosse C, Bard J, Bug W, Ceusters W, Goldberg LJ, Eilbeck K, Ireland A, Mungall CJ, Consortium TOBI, Leontis N, Rocca-Serra P, Ruttenberg A, Sansone S-A, Scheuermann RH, Shah N, Whetzel PL, Lewis S: The OBO Foundry: coordinated evolution of ontologies to support biomedical data integration. Nat Biotechnol 2007, 25:1251-1255.
• [23]Costa M, Reeve S, Grumbling G, Osumi-Sutherland D: The Drosophila anatomy ontology. J Biomed Sem 2013, 4:32. BioMed Central Full Text
• [24]Walls RL, Athreya B, Cooper L, Elser J, Gandolfo MA, Jaiswal P, Mungall CJ, Preece J, Rensing S, Smith B, Stevenson DW: Ontologies as integrative tools for plant science. Am J Bot 2012, 99:1263-1275.
• [25]Mungall CJ, Torniai C, Gkoutos GV, Lewis SE, Haendel MA: Uberon, an integrative multi-species anatomy ontology. Genome Biol 2012, 13:R5. BioMed Central Full Text
• [26]Domingo M, Martin-Baranera M, Sanz F, Sierra C, Uriz MJ: Validating SPONGIA, an expert system for sponge identification. Expert Syst Appl 1999, 16:379-384.
• [27]Haendel MA, Neuhaus F, Osumi-Sutherland D, Mabee PM, Mejino JLVJ, Mungall CJ, Smith B, Neuhaus DS: CARO - The Common Anatomy Reference Ontology. In Anatomy Ontologies for Bioinformatics: Principles and Practice. Edited by Burger A, Davidson D, Baldock R. Berline: Springer; 2007:1-23.
• [28]Müller WEG: The origin of metazoan complexity: Porifera as integrated animals. Integr Comp Biol 2003, 43:3-10.
• [29]Cárdenas P, Pérez T, Boury-Esnault N: Sponge systematics facing new challenges. Adv Mar Biol 2012, 61:79-209.
• [30]Bard J, Rhee S, Ashburner M: An ontology for cell types. Genome Biol 2005, 6:R21. BioMed Central Full Text
• [31]Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, et al.: The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726.
• [32]Hastings J, de Matos P, Dekker A, Ennis M, Harsha B, Kale N, Muthukrishnan V, Owen G, Turner S, Williams M, Steinbeck C: The ChEBI reference database and ontology for biologically relevant chemistry: enhancements for 2013. Nucleic Acids Res 2013, 41:D456-D463.
• [33]Gkoutos GV, Green EC, Mallon AM, Hancock JM, Davidson D: Using ontologies to describe mouse phenotypes. Genome Biol 2005, 6:R8. BioMed Central Full Text
• [34]Thacker RW, Hill AL, Hill MS, Redmond NE, Collins AG, Morrow CC, Spicer L, Carmack CA, Zappe ME, Pohlmann D, Hall C, Diaz MC, Bangalore PV: Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integr Comp Biol 2013, 53:373-387.
• [35]Wörheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C, Lavrov DV: Deep phylogeny and evolution of sponges (phylum Porifera). Adv Mar Biol 2012, 61:1-78.
• [36]Hooper JNA, Lévi C: Biogeography of Indo-west Pacific sponges: Microcionidae, Raspailiidae, Axinellidae. In Sponges in Time and Space. Edited by Van Soest RWM, Van Kempen TMG, Braekman JC. Rotterdam: Balkema; 1994:191-212.
• [37]Erwin PM, Thacker RW: Phylogenetic analyses of marine sponges within the order Verongida: a comparison of morphological and molecular data. Invertebr Biol 2007, 126:220-234.
• [38]Diaz MC, Thacker RW, Redmond NE, Matterson KO, Collins AG: Phylogenetic novelties and geographic anomalies among tropical Verongida. Integr Comp Biol 2013, 53:482-494.
• [39]Redmond NE, Morrow CC, Thacker RW, Diaz MC, Boury-Esnault N, Cárdenas P, Hajdu E, Lôbo-Hajdu G, Picton BE, Pomponi SA, Kayal E, Collins AG: Phylogeny and systematics of Demospongiae in light of new small-subunit ribosomal DNA (18S) sequences. Integr Comp Biol 2013, 53:388-415.
• [40]Morrow CC, Redmond NE, Picton BE, Thacker RW, Collins AG, Maggs CA, Sigwart JD, Allcock AL: Molecular phylogenies support homoplasy of multiple morphological characters used in the taxonomy of Heteroscleromorpha (Porifera: Demospongiae). Integr Comp Biol 2013, 53:428-446.
• [41]Morrow CC, Picton BE, Erpenbeck D, Boury-Esnault N, Maggs CA, Allcock AL: Congruence between nuclear and mitochondrial genes in Demospongiae: a new hypothesis for relationships within the G4 clade (Porifera: Demospongiae). Mol Phylogenet Evol 2012, 62:174-190.
• [42]Jones WC: Sheath and axial filament of calcareous sponge spicules. Nature 1967, 214:365-368.
• [43]Müller WE, Rothenberger M, Boreiko A, Tremel W, Reiber A, Schröder HC: Formation of silicieous spicules in the marine demosponge Suberites domuncula. Cell Tissue Res 2005, 321:285-297.
• [44]Franz NM, Goldstein AM: Phenotype ontologies: are homology relations central enough? A reply to Deans et al. Trends Ecol Evol 2013, 28:131-132.
• [45]Savarese M: Functional significance of regular archaeocyathan central cavity diameter: a biomechanical and paleoecological test. Paleobiology 1995, 21:356-378.
• [46]Kerner A, Debrenne F, Vignes-Lebbe R: Cambrian archaeocyathan metazoans: revision of morphological characters and standardization of genus descriptions to establish an online identification tool. Zookeys 2011, 150:381-395.
• [47]Bauer S, Sebastian K, Schulz MH, Robinson PN: Accurate and noise-tolerant searching in ontologies with frequency information. Bioinformatics 2012, 28:2502-2508.
• [48]Burleigh JG, Alphonse K, Alverson AJ, Bik HM, Blank C, Cirranello AL, Cui H, Daly M, Dietterich TG, Gasparich G, Irvine J, Julius M, Passarotti M, Law E, Moore L, Ranade S: Next-generation phenomics for the Tree of Life. PLOS Curr Tree Life 2013. doi:10.1371/currents.tol.085c713acafc8711b2ff7010a4b03733
• [49]Day-Richter J, Harris MA, Haendel M, Lewis S, Group GOO-EW: OBO-Edit - an ontology editor for biologists. Bioinformatics 2007, 23:2198-2200.
• [50]Horridge M, Tsarkov D, Redmond T: Supporting early adoption of OWL 1.1 with Protege-OWL and FaCT++. OWLED 2006. [http:www.webont.org/owled/2006/acceptedLong/submission_15.pdf webcite]
• [51]Shearer R, Motik B, Horrocks I: HermiT: A highly-efficient OWL reasoner. OWLED 2008. [http://www.cs.ox.ac.uk/boris.motik/pubs/smh08HermiT.pdf webcite]
• [52]Mungall CJ, Dietze H, Carbon SJ, Ireland A, Bauer S, Lewis S: Continuous Integration of Open Biological Ontology Libraries. 2012. [http://bio-ontologies.knowledgeblog.org/405 webcite]