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Sponge Digestive System Diversity and Evolution: Filter Feeding to Carnivory

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Sponge Digestive System Diversity and Evolution: Filter Feeding to Carnivory Sponge digestive system diversity and evolution: filter feeding to carnivory Nelly Godefroy, Emilie Le Goff, Camille Martinand-Mari, Khalid Belkhir, Jean Vacelet, Stephen Baghdiguian To cite this version: Nelly Godefroy, Emilie Le Goff, Camille Martinand-Mari, Khalid Belkhir, Jean Vacelet, et al.. Sponge digestive system diversity and evolution: filter feeding to carnivory. Cell and Tissue Research, Springer Verlag, 2019, 377 (3), pp.341-351. 10.1007/s00441-019-03032-8. hal-02296759 HAL Id: hal-02296759 https://hal-amu.archives-ouvertes.fr/hal-02296759 Submitted on 1 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Sponge digestive system diversity and evolution: filter feeding to carnivory Nelly Godefroy1 • Emilie Le Goff1 • Camille Martinand-Mari1 • Khalid Belkhir 1 • Jean Vacelet2 • Stephen Baghdiguian 1 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. Keywords Sponge . Porifera . Evolution . Choanocyte . Filtration . Carnivory Introduction asconoid organization to the most complex leuconoid and sole- noid filtration units (Fig. 1a). The great anatomical diversity of Sponges, or Porifera, are traditionally considered as one of the the five sponge organization plans raises a number of questions key groups for understanding basal metazoan evolution. The concerning which are the most ancestral and which are the most Porifera are a rich taxon of 8000 to 9000 described species, efficient in terms of filtration. But whatever the evolutionary currently divided into four monophyletic classes: history of the classic filtering sponge aquiferous system, these Demospongiae, Calcarea, Homoscleromorpha and, the most dif- different architectures, which aimed at optimizing food intake ferentiated form, the Hexactinellida. Despite the prevalent view by increasing the exchange surfaces of the filtration system with of sponges as Bsimple^ animals, they have very sophisticated the medium, never translated into a radical change in the general feeding mechanisms involving the whole body and including a organization of the body plan, unlike that which occurred in network of water filtration units, known as the aquiferous sys- carnivorous sponges (see below). In contrast to the diversity of tem. Studying the aquiferous system morphology of sponge Calcarea that possess the five types of body plan, in classes, subclasses, orders and suborders will show us a very Hexactinellida, only leuconoids and syconoids are observed. clear and interesting story of the successive modifications. Thus, All Homoscleromorpha are leuconoids, with a possible the system has various degrees of complexity from the simplest exception of Oscarella filipoi where a sylleibid system has been described in Perez and Ruiz (2018) and all the extant Demospongiae are leuconoids (Fig. 1c). It is likely that the evo- * Jean Vacelet lution in the class Calcarea (sponges characterized by calcareous [email protected] spicules) occurred by the complexification of the asconoid type * Stephen Baghdiguian into syconoid, sylleibid, leuconoid, or solenoid organization [email protected] (Cavalcanti and Klautau 2011). The same scenario can be con- sidered for the other three sponge classes with a secondary loss 1 ISEM, CNRS, EPHE, IRD, Univ Montpellier, Montpellier, France of asconoid, syconoid, sylleibid and/or solenoid forms. 2 IMBE, CNRS, IRD, Station Marine d’Endoume, Aix Marseille Univ, However, to date, there are no fossil remains or other evidence Univ Avignon, 13007 Marseille, France available to strengthen this hypothesis. Fig. 1 Sponge nutrition system anatomy. a Schematic representation of the arrow shows an additional exhalant orifice. c Phylogeny of the four the five sponge morphotypes. Arrows indicate the direction of the classes of sponges in relation to the presence + or absence − of the five seawater flow into the spongocoel or atrium (1) and out through the sponge morphotypes, (+) means that sylleibid organization was found oscule exhalant pore (2). In the more complex types, the water initially only in one species in Homoscleromorpha. d Scanning electron micros- passes through a choanocyte chamber (3). Note numbers are deliberately copy of representative spicules of filter/feeder sponges (upper panels) and faint to preserve the realism of the graphics. BGraphic design: ©Laurence carnivorous sponges (lower panels). Left upper panel: Palmate anisochela Meslin - CNRS 2018.^ b Scanning electron microscope view of Sycon from Mycale (Oxymycale klausjanusorum, Van Soest, 2018), Mycalidae sycandra. The upper left shows a whole specimen. The other micrographs (filtering sponges) (courtesy of Rob Van Soest). Left lower panel: Palmate show different sections obtained by cryo-fracture after double fixation in anisochela from an undescribed Asbestopluma, Cladorhizidae (carnivo- glutaraldehyde and osmium followed by ultra-fast congelation in liquid rous). Right upper panel: Placochela from Guitarra solorzanoi Cristobo, nitrogen and metallization. Micrographs illustrate the morphological or- 1998, Guitarridae (filtering sponges) (courtesy of Javier Cristobo). Right ganization of the syconoid system; sp, spicules; A ch, atrium chamber; T lower panel: Placochela from Euchelipluma pristina Topsent, 1909, ch c, tubular choanocyte chamber; ic, inhalant canals; in left upper panel, Cladorhizidae (carnivorous) Anatomical generalities bacteria increases with the density of this structure to maximize digestion (see the BInvolvement of the micro- The simplest of the five extant sponge plans, the asconoid form, biota in the carnivorous diet^ section). is found only in the smallest calcareous sponges such as Ascaltis, Clathrina and Leucosolenia. The asconoids are char- acterized by inhalant pores (or ostia) directly connected to the Nutrition/digestion in filtering sponges large central spongocoel cavity, which is lined with a monolayer of flagellated choanocytes. In syconoids, the choanocytes line a In filtering sponges, nutritive particles are mostly trapped by multitude of small radial channels rather than directly lining the flanges at the apical pole of choanocytes. Food particles are spongocoel (Fig. 1b). This organization plan was an evolution- intracellularly digested by lysosomal acid phosphatases, as ary advance because it increases the contact surface area be- well as by alpha glucosidases, beta hexosaminidases and ca- tween the cells of the animal and the surrounding water, thepsin D (Hahn-Keser and Stockem 1998). Cysteine protein- allowing greater absorption of food and increased body size. ases like cathepsin L were biochemically implicated in the The syconoid body plan is found among Calcarea, for instance, digestive process of Geodia cydonium also (Krasko et al. in the genera Grantessa, Sycon and Sycettusa. In the third form, 1997). After intravacuolar digestion, the nutritive vacuoles the sylleibids, the choanocyte chambers are radially arranged are exocytosed from choanocytes and delivered to pinacocytes around invaginations of the atrial cavity. The sylleibid body plan and archeocytes, which pass them on to another cell type via is found in Calcarea Leucilla, Leucandra and Jenkina genera. In the mesohyl space. Proof of this came when Ephydatia the fourth form, the leuconoids, which is the only form present fluviatilis were fed latex beads and the beads appeared in in all four classes of sponges, the choanocytes are collected in choanocytes after 10 min of incubation, in exopinacocytes elongated or spherical choanocyte chambers. These chambers after 20 min, in mesohyl and endopinacocytes after 40 min are not linked to each other, but rather they communicate with and finally in some archeocytes after up to 12 h (Willenz the spongocoel and ostia through channels. This organization 1980). Fluid pinocytosis is a type of endocytosis allowing has the effect of slowing down the inward flow, which the capture of macromolecules and solutes in small vesicles facilitates the filtration of the organic matter. This form that are redirected and incorporated into lysosomes. This kind is predominant in large calcareous sponges and essential- of endocytosis has been observed for beta glycogen and iron ly all of the demosponges, hexactinellids and saccharate transport in the leuconoid Demospongiae Suberites homoscleromorphs are leuconoid. In the fifth and final massa (Diaz 1979). Many questions relating to the precise
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