Skip to main content
Log in

Kinetid structure in larval and adult stages of the demosponges Haliclona aquaeductus (Haplosclerida) and Halichondria panicea (Suberitida)

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

Abstract

At larval and adult stage of life cycle, sponges (Porifera) have different flagellated cells that play different roles in their body. The larval epithelium cells serve as locomotion organs, while adult collar cells (choanocytes) have a feeding function. Here, for the first time, we describe detailed structure of the flagellar apparatus (kinetid) in larval cells and choanocytes of Haliclona aquaeductus and Halichondria panicea demosponges, and attach schemes of its organization, based on longitudinal and transversal ultrathin serial sections. The kinetid of larvae has proved to be more complicated than the choanocytes ones. It includes well-developed transverse and longitudinal cytoskeletons that strengthen the larval flagellum. The longitudinal skeleton in H. aquaeductus is represented by unusual structures, which were previously understudied: large tubular rootlets made of oblique-crossed fibers, which connect the kinetosome with mitochondria. We also found out that the kinetid composition varies between different cell types of a highly structured parenchymella of H. aquaeductus. In simply organized parenchymella of H. panicea, flagellated cells are identical and its kinetid includes a permanent additional centriole absent in choanocytes of adult sponges. We tried to evaluate the diversity of sponge larval kinetid organization based on literature data and found it variable within Haplosclerida and quite conservative within other sponge lineages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Amano S, Hori I (1992) Metamorphosis of calcareous sponges I. Ultrastructure of free-swimming larvae. Invertebr Reprod Dev 21:81–90. https://doi.org/10.1080/07924259.1992.9672223

    Article  Google Scholar 

  • Amano S, Hori I (1994) Metamorphosis of a demosponge I. Cells and structure of swimming larva. Invertebr Reprod Dev 25:193–204. https://doi.org/10.1080/07924259.1994.9672386

    Article  Google Scholar 

  • Amano S, Hori I (1996) Transdifferentiation of larval flagellated cells to choanocytes in the metamorphosis of the demosponge Haliclona permollis. Biol Bull 190:161–172

    Article  CAS  PubMed  Google Scholar 

  • Amano S, Hori I (2001) Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa. Biol Bull 200:20–32

    Article  CAS  PubMed  Google Scholar 

  • Andersen RA, Barr DJS, Lynn DH et al (1991) Terminology and nomenclature of the cytoskeletal elements with the flagellar/ciliary apparatus in protists. Protoplasma 164:1–8. https://doi.org/10.1007/BF01320809

    Article  Google Scholar 

  • Barr DJS (2001) Chytridiomycota. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The Mycota VII, Part A: systematics and evolution. Springer, Berlin, pp 93–112

    Chapter  Google Scholar 

  • Blum JJ (1971) Existence of a breaking point in cilia and flagella. J Theor Biol 22:257–263

    Article  Google Scholar 

  • Borojevic R (1969) Étude du développement et de la différenciation cellulaire d’éponges calcaires calcinèennes (genres Clathrina et Ascandra). Ann Embryol Morph 2:15–36

    Google Scholar 

  • Boury-Esnault N (1976) Ultrastructure de la larve parenchymella d’Hamigera hamigera (Schmidt) (Démosponge, Poecilosclerida). Origine des cellules grises. Cah Biol Mar 17:9–20

    Google Scholar 

  • Boury-Esnault N, Ereskovsky A, Bezac C, Tokina D (2003) Larval development in the Homoscleromorpha (Porifera, Demospongiae). Invertebr Biol 122:187–202

    Article  Google Scholar 

  • Chakrabarti A, Schatten H, Mitchell KD et al (1998) Chloral hydrate alters the organization of the ciliary basal apparatus and cell organelles in sea urchin embryos. Cell Tissue Res 293:453–462

    Article  CAS  PubMed  Google Scholar 

  • Ereskovsky AV (2010) The comparative embryology of sponges. Springer, London

    Book  Google Scholar 

  • Ereskovsky AV, Tokina DB (2004) Morphology and fine structure of the swimming larvae of Ircinia oros (Porifera, Demospongiae, Dictyoceratida). Invertebr Reprod Dev 45:137–150. https://doi.org/10.1080/07924259.2004.9652583

    Article  Google Scholar 

  • Ereskovsky AV, Willenz P (2008) Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127:175–187. https://doi.org/10.1007/s00435-008-0061-9

    Article  Google Scholar 

  • Evans CW (1977) The ultrastructure of larvae from the marine sponge Halichondria moorei Bergquist (Porifera, Demospongiae). Cah Biol Mar 13:427–433

    Google Scholar 

  • Gallissian M-F (1983) Etude ultrastructurale du developpement embryonnaire chez Grantia compressa F. (Porifera, Calcarea). Arch Anat Microsc 72:59–75

    CAS  Google Scholar 

  • Gallissian M-F, Vacelet J (1992) Ultrastructure of the oocyte and embryo of the calcified sponge, Petrobiona massiliana (Porifera, Calcarea). Zoomorphology 112:133–141

    Article  Google Scholar 

  • Gonobobleva EL (2007) Basal apparatus formation in external flagellated cells of Halisarca dujardini larvae (Demospongiae: Halisarcida) in the course of embryonic development. In: Porifera research: biodiversity, innovation and sustanability. pp 345–351

  • Ivanova L (1997) New data about morphology and metamorphosis of the spongillid larvae (Porifera, Spongillidae). 1. Morphology of the free-swimming larvae. Berliner geowiss Abh 20:55–71

    Google Scholar 

  • Karpov SA (2000) Flagellate phylogeny: ultrastructural approach. In: Leadbeater BS, Green JC (eds) The flagellates: unity, diversity and evolution. Taylor and Francis, London, pp 336–360

    Google Scholar 

  • Langenbruch PF, Jones CW (1990) Body structure of marine sponges. VI Choanocyte chamber structure in the Haplosclerida (Porifera, Demospongiae) and its relevance to the phylogenesis of the group. J Morphol 204:1–8

    Article  PubMed  Google Scholar 

  • Lanna E, Klautau M (2012) Embryogenesis and larval ultrastructure in Paraleucilla magna (Calcarea, Calcaronea), with remarks on the epilarval trophocyte epithelium ‘placental membrane’). Zoomorphology 131:277–292. https://doi.org/10.1007/s00435-012-0160-5

    Article  Google Scholar 

  • Leys SP, Degnan BM (2001) Cytological basis of photoresponsive behavior in a sponge larva. Biol Bull 201:323–338

    Article  CAS  PubMed  Google Scholar 

  • Leys SP, Degnan BM (2002) Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invertebr Biol 121:171–189

    Article  Google Scholar 

  • Mah JL, Leys SP (2017) Think like a sponge: the genetic signal of sensory cells in sponges. Dev Biol 431:93–100. https://doi.org/10.1016/j.ydbio.2017.06.012

    Article  CAS  PubMed  Google Scholar 

  • Maldonado M (2004) Choanoflagellates, choanocytes, and animal multicellularity. Invertebr Biol 123:1–22

    Article  Google Scholar 

  • Maldonado M (2006) The ecology of the sponge larva. Can J Zool 84:175–194. https://doi.org/10.1139/Z05-177

    Article  Google Scholar 

  • Maldonado M (2009) Embryonic development of verongid demosponges supports the independent acquisition of spongin skeletons as an alternative to the siliceous skeleton. Biol J Linn Soc 97:427–447. https://doi.org/10.1111/j.1095-8312.2009.01202.x

    Article  Google Scholar 

  • Maldonado M, Riesgo A (2008) Reproductive output in a Mediterranean population of the homosclerophorid Corticium candelabrum (Porifera, Demospongiae), with notes on the ultrastructure and behavior of the larva. Mar Ecol 29:298–316. https://doi.org/10.1111/j.1439-0485.2008.00244.x

    Article  Google Scholar 

  • Maldonado M, Durfort M, McCarthy DA, Young CM (2003) The cellular basis of photobehavior in the tufted parenchymella larva of demosponges. Mar Biol 143:427–441. https://doi.org/10.1007/s00227-003-1100-1

    Article  Google Scholar 

  • Moestrup Ø (1982) Flagellar structure in algae: a review, with new observations particularly on the Chrysophyceae, Phaeophyceae (Fucophyceae), Euglenophyceae, and Reckertia. Phycologia 21:427–528

    Article  Google Scholar 

  • Moestrup Ø (2000) The flagellate cytoskeleton: introduction of a general terminology for microtubular roots in protists. In: Leadbeater BS, Green JC (eds) The flagellates: unity, diversity and evolution. Taylor and Francis, London, pp 69–94

    Google Scholar 

  • Morrow C, Cárdenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front Zool. https://doi.org/10.1186/s12983-015-0099-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakanishi N, Sogabe S, Degnan BM (2014) Evolutionary origin of gastrulation: insights from sponge development. BMC Biol 12:1–9. https://doi.org/10.1186/1741-7007-12-26

    Article  CAS  Google Scholar 

  • Nakanishi N, Stoupin D, Degnan SM, Degnan BM (2015) Integrative and comparative biology sensory flask cells in sponge larvae regulate metamorphosis via calcium signaling. Integr Comp Biol 55:1018–1027. https://doi.org/10.1093/icb/icv014

    Article  CAS  PubMed  Google Scholar 

  • Nielsen C (1987) Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zool 68:205–262. https://doi.org/10.1111/j.1463-6395.1987.tb00892.x

    Article  Google Scholar 

  • Pozdnyakov IR, Karpov SA (2013) Flagellar apparatus structure of choanocyte in Sycon sp. and its significance for phylogeny of Porifera. Zoomorphology 132:351–357. https://doi.org/10.1007/s00435-013-0193-4

    Article  Google Scholar 

  • Pozdnyakov IR, Karpov SA (2015) Structure of choanocyte’s kinetid in sponge Haliclona sp. (Demospongiae, Haplosclerida) and its implication for taxonomy and phylogeny of Demospongiae. Zool Zhurnal 94:17–25. https://doi.org/10.7868/S0044513415010122

    Article  Google Scholar 

  • Pozdnyakov IR, Karpov SA (2016) Kinetid structure in choanocytes of sponges (Heteroscleromorpha): toward the ancestral kinetid of Demospongiae. J Morphol 277:925–934. https://doi.org/10.1002/jmor.20546

    Article  PubMed  Google Scholar 

  • Pozdnyakov IR, Sokolova AM, Ereskovsky AV, Karpov SA (2017) Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship. Protistology 11:248–264. https://doi.org/10.21685/1680-0826-2017-11-4-6

    Article  Google Scholar 

  • Pozdnyakov IR, Sokolova AM, Ereskovsky AV, Karpov SA (2018) Kinetid structure in sponge choanocytes of Spongillida in the light of evolutionary relationships within Demospongiae. Zool J Linn Soc XX:1–18. https://doi.org/10.1093/zoolinnean/zlx109/4905843

    Article  Google Scholar 

  • Redmond NE, Raleigh J, Soest RWM, Van et al (2011) Phylogenetic relationships of the marine Haplosclerida (phylum Porifera) employing ribosomal (28S rRNA) and mitochondrial (cox1, nad1) gene sequence data. PLoS One 6:e24344. https://doi.org/10.1371/journal.pone.0024344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simion P, Philippe H, Baurain D, Jager M et al (2017) A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol 27(7):958–967. https://doi.org/10.1016/j.cub.2017.02.031

    Article  CAS  PubMed  Google Scholar 

  • Stephens K (2013) Insights into the evolution and development of H. indistincta (Porifera, Haplosclerida). Dissertation, National University of Ireland, Galway

  • Stephens KM, Ereskovsky AV, Lalor P, Mccormack GP (2013) Ultrastructure of the ciliated cells of the free-swimming larva, and sessile stages, of the marine sponge Haliclona indistincta (Demospongiae: Haplosclerida). J Exp Mar Bio Ecol 274:1263–1276. https://doi.org/10.1002/jmor.20177

    Article  Google Scholar 

  • Uriz MJ, Turon X, Becerro MA (2001) Morphology and ultrastructure of the swimming larvae of Crambe crambe (Demospongiae, Poecilosclerida). Invertebr Biol 120:295–307

    Article  Google Scholar 

  • Uriz MJ, Turon X, Mariani S (2008) Ultrastructure and dispersal potential of sponge larvae: tufted versus evenly ciliated parenchymellae. 29:280–297. https://doi.org/10.1111/j.1439-0485.2008.00229.x

  • Usher KM, Ereskovsky AV (2005) Larval development, ultrastructure and metamorphosis in Chondrilla australiensis Carter, 1873 (Demospongiae, Chondrosida, Chondrillidae). Invertebr Reprod Dev 47:51–62. https://doi.org/10.1080/07924259.2005.9652146

    Article  Google Scholar 

  • Woollacott RM (1990) Structure and swimming behavior of the larva of Halichondria melanadocia (Porifera: Demospongiae). J Morphol 205:135–145

    Article  PubMed  Google Scholar 

  • Woollacott RM (1993) Structure and swimming behavior of the larva of Haliclona tubifera (Porifera: Demospongiae). J Morphol 218:301–321

    Article  PubMed  Google Scholar 

  • Woollacott RM, Pinto RL (1995) Flagellar basal apparatus and its utility in phylogenetic analyses of the Porifera. J Morphol 226:247–265

    Article  PubMed  Google Scholar 

  • Yubuki N, Leander BS (2013) Evolution of microtubule organizing centers across the tree of eukaryotes. Plant J 75:230–244

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The research was supported by the Russian Foundation for Basic Research (projects nos. 17-304-50015 and 18-04-01314). We thank Research Resource Center for Microscopy at Zoological Institute of Russian Academy of Sciences and Research Resource Center for Molecular and Cell Technologies (RRC MCT) at St. Petersburg State University for access to the EM facilities. We are also grateful to A. B. Tsetlin and personnel of White Sea Biological station (WSBS MSU) for assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Agniya M. Sokolova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

We neither used endangered species nor were the investigated animals collected in protected areas. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Informed consent

Informed consent was obtained from all the individual participants included in the study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sokolova, A.M., Pozdnyakov, I.R., Ereskovsky, A.V. et al. Kinetid structure in larval and adult stages of the demosponges Haliclona aquaeductus (Haplosclerida) and Halichondria panicea (Suberitida). Zoomorphology 138, 171–184 (2019). https://doi.org/10.1007/s00435-019-00437-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-019-00437-5

Keywords

Navigation