Abstract
Sponges are an ancient basal life form, so understanding their evolution is key to understanding all metazoan evolution. Sponges have very unusual feeding mechanisms, with an intricate network of progressively optimized filtration units: from the simple choanocyte lining of a central cavity, or spongocoel, to more complex chambers and canals. Furthermore, in a single evolutionary event, a group of sponges transitioned to carnivory. This major evolutionary transition involved replacing the filter-feeding apparatus with mobile phagocytic cells that migrate collectively towards the trapped prey. Here, we focus on the diversity and evolution of sponge nutrition systems and the amazing adaptation to carnivory.
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References
Bergquist PR (1978) Sponges. Hutchinson, London & University of California Press, Berkeley & Los Angeles, pp 1–268
Cavalcanti FF, Klautau M (2011) Solenoid: a new aquiferous system to Porifera. Zoomorphology 130:255–260. https://doi.org/10.1007/s00435-011-0139-7
Cavalier-Smith T (2017) Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion. Philos Trans R Soc B 372:20150476. https://doi.org/10.1098/rstb.2015.0476
Diaz J (1979) Variations, différenciations et fonctions des catégories cellulaires de la démosponge d’eaux saumâtres, Suberites massa Nardo, au cours du cycle biologique annuel et dans des conditions expérimentales. Docteur d’Etat Mention Sciences, Université des sciences et techniques du Languedoc
Dupont S, Corre E, Li Y et al (2013) First insights into the microbiome of a carnivorous sponge. FEMS Microbiol Ecol 86:520–531. https://doi.org/10.1111/1574-6941.12178
Dupont S, Carre-Mlouka A, Domart-Coulon I et al (2014) Exploring cultivable Bacteria from the prokaryotic community associated with the carnivorous sponge Asbestopluma hypogea. FEMS Microbiol Ecol 88:160–174. https://doi.org/10.1111/1574-6941.12279
Fukushima K, Fang X, Alvarez-Ponce D et al (2017) Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nat Ecol Evolut 1:0059. https://doi.org/10.1038/s41559-016-0059
Funayama N (2013) The stem cell system in demosponges: suggested involvement of two types of cells: archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells). Dev Genes Evol 223:23–38. https://doi.org/10.1007/s00427-012-0417-5
Gober JW, Alley MR, Shapiro L (1991) Positional information during Caulobacter cell differentiation. Curr Opin Genet Dev 1:324–329
Hahn-Keser B, Stockem W (1998) Intracellular pathways and degradation of endosomal contents in basal epithelial cells of freshwater sponges (Porifera, Spongillidae). Zoomorphology 117:223–236. https://doi.org/10.1007/s004350050047
Hestetun JT, Dahle H, Jørgensen SL et al (2016) The microbiome and occurrence of methanotrophy in carnivorous sponges. Front Microbiol 7:1781. https://doi.org/10.3389/fmicb.2016.01781
Hestetun JT, Tompkins-Macdonald G, Rapp HT (2017) A review of carnivorous sponges (Porifera: Cladorhizidae) from the boreal North Atlantic and Arctic. Zool J Linnean Soc 181:1–69. https://doi.org/10.1093/zoolinnean/zlw022
Krasko A, Gamulin V, Seack J et al (1997) Cathepsin, a major protease of the marine sponge Geodia cydonium: purification of the enzyme and molecular cloning of cDNA. Mol Mar Biol Biotechnol 6:296–307
Leys SP, Mackie GO, Reiswig HM (2007) The biology of glass sponges. Adv Mar Biol 52:1–145. https://doi.org/10.1016/S0065-2881(06)52001-2
Martinand-Mari C, Vacelet J, Nickel M et al (2012) Cell death and renewal during prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Poecilosclerida). J Exp Biol 215:3937–3943. https://doi.org/10.1242/jeb.072371
Monniot C, Monniot F (1975) Abyssal tunicates: an ecological paradox. Ann Inst océanogr 51(1):99–129
Monniot C, Monniot F (1991) Découverte d’une nouvelle lignée évolutive chez les ascidies de grande profondeur : une Ascidiidae carnivore. C R Acad Sci Paris III:383–388
Perez T, Ruiz C (2018) Description of the first Caribbean Oscarellidae (Porifera: Homoscleromorpha). Zootaxa 4369:501–514. https://doi.org/10.11646/zootaxa.4369.4.3
Pett W, Adamski M, Adamska M et al (2019) The role of homology and orthology in the phylogenomic analysis of metazoan gene content. Mol Biol Evol. https://doi.org/10.1093/molbev/msz013
Riesgo A, Taylor C, Leys SP (2007) Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan. Evol Dev 9:618–631. https://doi.org/10.1111/j.1525-142X.2007.00200.x
Simion P, Philippe H, Baurain D et al (2017) A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol 27:958–967. https://doi.org/10.1016/j.cub.2017.02.031
Srivastava M, Simakov O, Chapman J et al (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726. https://doi.org/10.1038/nature09201
Vacelet J, Boury-Esnault N (1995) Carnivorous sponges. Nature 373(6512):333–335
Vacelet J, Duport E (2004) Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae). Zoomorphology 123:179–190. https://doi.org/10.1007/s00435-004-0100-0
Verhoeven JTP, Dufour SC (2017) Microbiomes of the Arctic carnivorous sponges Chondrocladia grandis and Cladorhiza oxeata suggest a specific, but differential involvement of bacterial associates. Arctic Sci 4:186–204. https://doi.org/10.1139/as-2017-0015
Willenz P (1980) Kinetic and morphological aspect of particle ingestion by the freshwater sponge Ephydatia fluviatilis L. In: Smith DC, Tiffon Y (eds) Nutrition in the lower Metazoa. Pergamon Press, Oxford & New York
Acknowledgments
We thank Laurence Meslin (CNRS, “Plateforme Communication Scientifique Visuelle – ISEM”), for the drawing and elaborating the figures. For the transcriptomic data, we benefited from the Montpellier Bioinformatics Biodiversity platform supported by the LabEx CeMEB, an ANR “Investissements d’avenir” program (ANR-10-LABX-04-01).
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Godefroy, N., Le Goff, E., Martinand-Mari, C. et al. Sponge digestive system diversity and evolution: filter feeding to carnivory. Cell Tissue Res 377, 341–351 (2019). https://doi.org/10.1007/s00441-019-03032-8
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DOI: https://doi.org/10.1007/s00441-019-03032-8