Structure of putative epidermal sensory receptors in an acoel flatworm, Praesagittifera naikaiensis.

Phalloidin Polycystin Xenacoelomorpha dSap47 α-Tubulin

Journal

Cell and tissue research
ISSN: 1432-0878
Titre abrégé: Cell Tissue Res
Pays: Germany
ID NLM: 0417625

Informations de publication

Date de publication:
02 Feb 2024
Historique:
received: 28 07 2023
accepted: 08 01 2024
medline: 2 2 2024
pubmed: 2 2 2024
entrez: 2 2 2024
Statut: aheadofprint

Résumé

Acoel flatworms possess epidermal sensory-receptor cells on their body surfaces and exhibit behavioral repertoires such as geotaxis and phototaxis. Acoel epidermal sensory receptors should be mechanical and/or chemical receptors; however, the mechanisms of their sensory reception have not been elucidated. We examined the three-dimensional relationship between epidermal sensory receptors and their innervation in an acoel flatworm, Praesagittifera naikaiensis. The distribution of the sensory receptors was different between the ventral and dorsal sides of worms. The nervous system was mainly composed of a peripheral nerve net, an anterior brain, and three pairs of longitudinal nerve cords. The nerve net was located closer to the body surface than the brain and the nerve cords. The sensory receptors have neural connections with the nerve net in the entire body of worms. We identified five homologs of polycystic kidney disease (PKD): PKD1-1, PKD1-2, PKD1-3, PKD1-4, and, PKD2, from the P. naikaiensis genome. All of these PKD genes were implied to be expressed in the epidermal sensory receptors of P. naikaiensis. PKD1-1 and PKD2 were dispersed across the entire body of worms. PKD1-2, PKD1-3, and PKD1-4 were expressed in the anterior region of worms. PKD1-4 was also expressed around the mouth opening. Our results indicated that P. naikaiensis possessed several types of epidermal sensory receptors to convert various environmental stimuli into electrical signals via the PKD channels and transmit the signals to afferent nerve and/or effector cells.

Identifiants

pubmed: 38305882
doi: 10.1007/s00441-024-03865-y
pii: 10.1007/s00441-024-03865-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Japan Society for the Promotion of Science
ID : 22KJ2308
Organisme : Research Institute of Marine Invertebrates
ID : KO2021-05

Informations de copyright

© 2024. The Author(s).

Références

Achatz JG, Martinez P (2012) The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications. Front Zool 9:27. https://doi.org/10.1186/1742-9994-9-27
doi: 10.1186/1742-9994-9-27 pubmed: 23072457 pmcid: 3488495
Achatz JG, Chiodin M, Salvenmoser W, Tyler S, Martinez P (2013) The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis). Org Divers Evol 13:267–286. https://doi.org/10.1007/s13127-012-0112-4
doi: 10.1007/s13127-012-0112-4 pubmed: 24098090
Arboleda E, Hartenstein V, Martinez P, Reichert H, Sen S, Sprecher S, Bailly X (2018) An emerging system to study photosymbiosis, brain regeneration, chronobiology, and behavior: the marine Acoel Symsagittifera roscofensis. BioEssays 40:1800107. https://doi.org/10.1002/bies.201800107
doi: 10.1002/bies.201800107
Arimoto A, Hikosaka-Katayama T, Hikosaka A, Tagawa K, Inoue T, Ueki T, Yoshida M, Kanda M, Shoguchi E, Hisata K, Satoh N (2019) A draft nuclear-genome assembly of the acoel flatworm Praesagittifera naikaiensis. GigaScience 8:giz023. https://doi.org/10.1093/gigascience/giz023
Barr MM (2005) Caenorhabditis elegans as a model to study renal development and disease: sexy cilia. J Am Soc Nephrol 16:305–312. https://doi.org/10.1681/ASN.2004080645
doi: 10.1681/ASN.2004080645 pubmed: 15647338
Barr MM, Sternberg PW (1999) A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386–389. https://doi.org/10.1038/43913
doi: 10.1038/43913 pubmed: 10517638
Bedini C, Lanfranchi A (1991) The central and peripheral nervous system of Acoela (Plathelminthes). An Electron Microscopical Study Acta Zool 72:101–106. https://doi.org/10.1111/j.1463-6395.1991.tb00322.x
doi: 10.1111/j.1463-6395.1991.tb00322.x
Bedini C, Ferrero E, Lanfranchi A (1973) The ultrastructure of ciliary sensory cells in two Turbellaria Acoela. Tissue Cell 5:359–372. https://doi.org/10.1016/S0040-8166(73)80030-8
doi: 10.1016/S0040-8166(73)80030-8 pubmed: 4744676
Bery A, Cardona A, Martinez P, Hartenstein V (2010) Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev Genes Evol 220:61–76. https://doi.org/10.1007/s00427-010-0328-2
doi: 10.1007/s00427-010-0328-2 pubmed: 20549514 pmcid: 2929339
Bezares-Calderón LA, Berger J, Jékely G (2020) Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour. Phil Trans R Soc B 375:20190376. https://doi.org/10.1098/rstb.2019.0376
doi: 10.1098/rstb.2019.0376 pubmed: 31884914
Brusca RC, Moore W, Shuster SM (2016) Invertebrates, 3rd edn. Sinauer Associates, Massachusetts
Cannon JT, Vellutini BC, Smith J, Ronquist F, Jondelius U, Hejnol A (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530:89–93. https://doi.org/10.1038/nature16520
doi: 10.1038/nature16520 pubmed: 26842059
Cribb B, Chisholm L, Gould R, Whittington I (2003) Morphology, ultrastructure, and implied function of ciliated sensory structures on the developmental stages of Merizocotyle icopae (Monogenea: Monocotylidae). Microsc Res Tech 62:267–276. https://doi.org/10.1002/jemt.10387
doi: 10.1002/jemt.10387 pubmed: 14506693
Dupont S, Moya A, Bailly X (2012) Stable photosymbiotic relationship under CO
doi: 10.1371/journal.pone.0029568 pubmed: 22253736 pmcid: 3253794
Duruz J, Kaltenrieder C, Ladurner P, Bruggmann R, Martìnez P, Sprecher SG (2021) Acoel single-cell transcriptomics: cell type analysis of a deep branching bilaterian. Mol Biol Evol 38:1888–1904. https://doi.org/10.1093/molbev/msaa333
doi: 10.1093/molbev/msaa333 pubmed: 33355655
Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763. https://doi.org/10.1093/bioinformatics/14.9.755
doi: 10.1093/bioinformatics/14.9.755 pubmed: 9918945
Esarte Palomero O, Larmore M, DeCaen PG (2023) Polycystin channel complexes. Annu Rev Physiol 85:425–448. https://doi.org/10.1146/annurev-physiol-031522-084334
doi: 10.1146/annurev-physiol-031522-084334 pubmed: 36763973
Ferrero E (1973) A fine structural analysis of the statocyst in Turbellaria Acoela. Zool Scr 2:5–16. https://doi.org/10.1111/j.1463-6409.1973.tb00793.x
doi: 10.1111/j.1463-6409.1973.tb00793.x
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
doi: 10.1093/nar/gkv1344 pubmed: 26673716
Gamble FW, Keeble F (1904) The bionomics of Convoluta roscoffensis, with special reference to its green cells. Proc R Soc Lond 72:93–98. https://doi.org/10.1098/rspl.1903.0022
doi: 10.1098/rspl.1903.0022
Gao Z, Ruden DM, Lu X (2003) PKD2 cation channel is required for directional sperm movement and male fertility. Curr Biol 13:2175–2178. https://doi.org/10.1016/j.cub.2003.11.053
doi: 10.1016/j.cub.2003.11.053 pubmed: 14680633
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hikosaka-Katayama T, Watanuki N, Niiho S, Hikosaka A (2020) Geographical distribution and genetic diversity of Praesagittifera naikaiensis (Acoelomorpha) in the Seto Inland Sea, Japan. Zool Sci 37:314–322. https://doi.org/10.2108/zs190119
doi: 10.2108/zs190119
Hulett RE, Kimura JO, Bolaños DM, Luo YJ, Ricci L, Srivastava M (2022) Acoel single-cell atlas reveals expression dynamics and heterogeneity of a pluripotent stem cell population. BioRxiv 2022–02. https://doi.org/10.1101/2022.02.10.479464
Jennings JB (1957) Studies on feeding, digestion, and food storage in free-living flatworms (Platyhelminthes: Turbellaria). Biol Bull 112:63–80. https://doi.org/10.2307/1538879
doi: 10.2307/1538879
Jondelius U, Wallberg A, Hooge M, Raikova OI (2011) How the worm got its pharynx: phylogeny, classification and Bayesian assessment of character evolution in Acoela. Syst Biol 60:845–871. https://doi.org/10.1093/sysbio/syr073
doi: 10.1093/sysbio/syr073 pubmed: 21828080
Keeble F (1912) Plant-animals: a study in symbiosis. Cambridge University Press, London
Köttgen M, Buchholz B, Garcia-Gonzalez MA, Kotsis F, Fu Z, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T, Nitschke R, Suzuki M, Kramer-Zucker A, Germino GG, Watnick T, Prenen J, Nilius B, Kuehn EW, Walz G (2008) TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182:437–447. https://doi.org/10.1083/jcb.200805124
doi: 10.1083/jcb.200805124 pubmed: 18695040 pmcid: 2500130
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
doi: 10.1093/bioinformatics/btm404 pubmed: 17846036
Marlétaz F, Peijnenburg KT, Goto T, Satoh N, Rokhsar DS (2019) A new spiralian phylogeny places the enigmatic arrow worms among gnathiferans. Curr Biol 29:312–318. https://doi.org/10.1016/j.cub.2018.11.042
doi: 10.1016/j.cub.2018.11.042 pubmed: 30639106
Martinez P, Hartenstein V, Sprecher S (2017) Xenacoelomorpha nervous systems. Oxford Research Encyclopedia of Neuroscience. https://doi.org/10.1093/acrefore/9780190264086.013.203
doi: 10.1093/acrefore/9780190264086.013.203
Martinez P, Hartenstein V, Gavilán B, Sprecher SG, Bailly X (2021) Symsagittifera roscoffensis as a model in biology. In: Boutet A, Schierwater B (eds) Handbook of marine model organisms in experimental biology, 1st edn. CRC Press, Florida, pp 217–234
doi: 10.1201/9781003217503-12
McGrath J, Somlo S, Makova S, Tian X, Brueckner M (2003) Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114:61–73. https://doi.org/10.1016/S0092-8674(03)00511-7
doi: 10.1016/S0092-8674(03)00511-7 pubmed: 12859898
McLaughlin S (2017) Evidence that polycystins are involved in Hydra cnidocyte discharge. Invertebr Neurosci 17:1–14. https://doi.org/10.1007/s10158-016-0194-3
doi: 10.1007/s10158-016-0194-3
Mulhair PO, McCarthy CG, Siu-Ting K, Creevey CJ, O’Connell MJ (2021) Enriching for orthologs increases support for Xenacoelomorpha and Ambulacraria sister relationship. BioRxiv 2021–12.
Nissen M, Shcherbakov D, Heyer A, Brummer F, Schill RO (2015) Behaviour of the plathelminth Symsagittifera roscoffensis under different light conditions and the consequences for the symbiotic algae Tetraselmis convolutae. J Exp Biol 218:1693–1698. https://doi.org/10.1242/jeb.110429
doi: 10.1242/jeb.110429 pubmed: 25852067
Nonaka S, Shiratori H, Saijoh Y, Hamada H (2002) Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418:96–99. https://doi.org/10.1038/nature00849
doi: 10.1038/nature00849 pubmed: 12097914
Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369. https://doi.org/10.1016/0300-9084(96)84768-7
doi: 10.1016/0300-9084(96)84768-7 pubmed: 8905155
Pfistermüller R, Tyler S (2002) Correlation of fluorescence and electron microscopy of F-actin-containing sensory cells in the epidermis of Convoluta pulchra (Platyhelminthes: Acoela). Acta Zool 83:15–24. https://doi.org/10.1046/j.1463-6395.2002.00095.x
doi: 10.1046/j.1463-6395.2002.00095.x
Philippe H, Poustka AJ, Chiodin M, Hoff KJ, Dessimoz C, Tomiczek B, Schiffer PH, Müller S, Domman D, Horn M, Kuhl H, Timmermann B, Satoh N, Hikosaka-Katayama T, Nakano H, Rowe ML, Elphick MR, Thomas-Chollier M, Hankeln T, Mertes F, Wallberg A, Copley RR, Martinez P, Telford MJ (2019) Mitigating anticipated effects of systematic errors supports sister-group relationship between Xenacoelomorpha and Ambulacraria. Curr Biol 29:1818–1826. https://doi.org/10.1016/j.cub.2019.04.009
doi: 10.1016/j.cub.2019.04.009 pubmed: 31104936
Praetorius HA, Spring KR (2003a) Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 191:69–76. https://doi.org/10.1007/s00232-002-1042-4
doi: 10.1007/s00232-002-1042-4 pubmed: 12532278
Praetorius HA, Spring KR (2003b) The renal cell primary cilium functions as a flow sensor. Curr Opin Nephrol Hypertens 12:517–520. https://doi.org/10.1097/01.mnh.0000088730.87142.d1
doi: 10.1097/01.mnh.0000088730.87142.d1 pubmed: 12920399
Raikova OI, Reuter M, Kotikova EA, Gustafsson MK (1998) A commissural brain! The pattern of 5-HT immunoreactivity in Acoela (Plathelminthes). Zoomorphology 118:69–77. https://doi.org/10.1007/s004350050058
doi: 10.1007/s004350050058
Reichmuth C, Becker S, Benz M, Debel K, Reisch D, Heimbeck G, Hofbauer A, Klagges B, Pflugfelder GO, Buchner E (1995) The sap47 gene of Drosophila melanogaster codes for a novel conserved neuronal protein associated with synaptic terminals. Mol Brain Res 32:45–54. https://doi.org/10.1016/0169-328X(95)00058-Z
doi: 10.1016/0169-328X(95)00058-Z pubmed: 7494462
Rieger RM, Tyler S, Smith JPS, Rieger GE (1991) Platyhelminthes: Turbellaria. In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates, vol 3. Wiley-Liss, New York, pp 7–140
Sakagami T, Watanabe K, Ikeda R, Ando M (2021) Structural analysis of the statocyst and nervous system of Praesagittifera naikaiensis, an acoel flatworm, during development after hatching. Zoomorphology 140:183–192. https://doi.org/10.1007/s00435-021-00521-9
doi: 10.1007/s00435-021-00521-9
Semmler H, Bailly X, Wanninger A (2008) Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela). Front Zool 5:14. https://doi.org/10.1186/1742-9994-5-14
doi: 10.1186/1742-9994-5-14 pubmed: 18803837 pmcid: 2562460
Sprecher SG, Bernardo-Garcia FJ, van Giesen L, Hartenstein V, Reichert H, Neves R, Bailly X, Martinez P, Brauchle M (2015) Functional brain regeneration in the acoel worm Symsagittifera roscoffensis. Biol Open 4:1688–1695. https://doi.org/10.1242/bio.014266
doi: 10.1242/bio.014266 pubmed: 26581588 pmcid: 4736034
Todt C, Tyler S (2007) Ciliary receptors associated with the mouth and pharynx of Acoela (Acoelomorpha): a comparative ultrastructural study. Acta Zool 88:41–58. https://doi.org/10.1111/j.1463-6395.2007.00246.x
doi: 10.1111/j.1463-6395.2007.00246.x
Tyler S (1984) Turbellarian platyhelminths. In: Bereiter-Hahn J, Matoltsy S, Richards KS (eds) Biology of the integument, vol 1. Springer-Verlag, Berlin, pp 112–131
doi: 10.1007/978-3-642-51593-4_10
Tyler S, Rieger RM (1999) Functional morphology of musculature in the acoelomate worm, Convoluta pulchra (Plathelminthes). Zoomorphology 119:127–142. https://doi.org/10.1007/s004350050087
doi: 10.1007/s004350050087
Watnick TJ, Jin Y, Matunis E, Kernan MJ, Montell C (2003) A flagellar polycystin-2 homolog required for male fertility in Drosophila. Curr Biol 13:2179–2184. https://doi.org/10.1016/j.cub.2003.12.002
doi: 10.1016/j.cub.2003.12.002 pubmed: 14680634
Watson NA, Rohde K (1994) Two new sensory receptors in Gyrodactylus sp. (Platyhelminthes, Monogenea, Monopisthocotylea). Parasitol Res 80:442–445. https://doi.org/10.1007/BF00932385
doi: 10.1007/BF00932385 pubmed: 7971933
Whittington IA, Chisholm LA, Rohde K (1999) The larvae of Monogena (Platyhelminthes). Adv Parasitol 44:141–232. https://doi.org/10.1016/S0065-308X(08)60232-8
doi: 10.1016/S0065-308X(08)60232-8
Yamasu T (1982) Five new species of acoel flat worms from Japan. Galaxea 1:29–43
Yamasu T (1991) Fine structure and function of ocelli and sagittocysts of acoel flatworms. Hydrobiol 227:273–282. https://doi.org/10.1007/BF00027612
doi: 10.1007/BF00027612
Zabotin YI (2019) Ultrastructure of epidermal sensillae in three species of Acoela. Invert Zool 16:71–77. https://doi.org/10.15298/invertzool.16.1.08
Zabotin YI, Evtugyn VG (2021) Ultrastructure of spermatozoa and female copulatory organs in preferably asexually-reproducing acoel Convolutriloba retrogemma (Acoelomorpha). Zoomorphology 140:19–26. https://doi.org/10.1007/s00435-020-00505-1
doi: 10.1007/s00435-020-00505-1
Zabotin YI, Golubev AI (2014) Ultrastructure of oocytes and female copulatory organs of Acoela. Biol Bull Russ Acad Sci 41:722–735. https://doi.org/10.1134/S106235901409009X
doi: 10.1134/S106235901409009X

Auteurs

Tosuke Sakagami (T)

Laboratory of Animal Physiology and Pharmacology, Department of Animal Science, Graduate School of Environmental and Life Science, Okayama University, Okayama, 700-8530, Japan.

Kaho Watanabe (K)

Laboratory of Cell Physiology, Department of Science Education, Graduate School of Education, Okayama University, Okayama, 700-8530, Japan.

Mayuko Hamada (M)

Ushimado Marine Institute, Graduate School of Natural Science and Technology, Okayama University, Okayama, 701-4303, Japan.

Tatsuya Sakamoto (T)

Ushimado Marine Institute, Graduate School of Natural Science and Technology, Okayama University, Okayama, 701-4303, Japan.

Toshimitsu Hatabu (T)

Laboratory of Animal Physiology and Pharmacology, Department of Animal Science, Graduate School of Environmental and Life Science, Okayama University, Okayama, 700-8530, Japan.

Motonori Ando (M)

Laboratory of Animal Physiology and Pharmacology, Department of Animal Science, Graduate School of Environmental and Life Science, Okayama University, Okayama, 700-8530, Japan. andom@okayama-u.ac.jp.
Laboratory of Cell Physiology, Department of Science Education, Graduate School of Education, Okayama University, Okayama, 700-8530, Japan. andom@okayama-u.ac.jp.

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