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Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis

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Abstract

From a morphological point of view, placozoans are among the most simple free-living animals. This enigmatic phylum is critical for our understanding of the evolution of animals and their cell types. Their millimeter-sized, disc-like bodies consist of only three cell layers that are shaped by roughly seven major cell types. Placozoans lack muscle cells and neurons but are able to move using their ciliated lower surface and take up food in a highly coordinated manner. Intriguingly, the genome of Trichoplax adhaerens, the founding member of the enigmatic phylum, has disclosed a surprising level of genetic complexity. Moreover, recent molecular and functional investigations have uncovered a much larger, so-far hidden cell-type diversity. Here, we have extended the microanatomical characterization of a recently described placozoan species—Hoilungia hongkongensis. In H. hongkongensis, we recognized the established canonical three-layered placozoan body plan but also came across several morphologically distinct and potentially novel cell types, among them novel gland cells and “shiny spheres”-bearing cells at the upper epithelium. Thus, the diversity of cell types in placozoans is indeed higher than anticipated.

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The data that support the findings of this study are available on https://zenodo.org.

References

  • Arendt D (2020) The evolutionary assembly of neuronal machinery. Curr Biol 30(10):R603–R616

    Article  CAS  PubMed  Google Scholar 

  • Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C, Erwin DH, Pavlicev M, Schlosser G, Widder S, Laubichler MD, Wagner GP (2016) The origin and evolution of cell types. Nat Rev Genet 17(12):744–757

    Article  CAS  PubMed  Google Scholar 

  • Armon S, Bull MS, Aranda-Diaz A, Prakash M (2018) Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity. Proc Natl Acad Sci USA 115(44):E10333–E10341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ball EE, Miller DJ (2010) Putting placozoans on the (phylogeographic) map. Mol Ecol 19(11):2181–2183

    Article  PubMed  Google Scholar 

  • Behrendt G, Ruthmann A (1986) The cytoskeleton of the fiber cells of Trichoplax adhaerens (Placozoa). Zoomorphology 106(2):123130

    Article  Google Scholar 

  • Birchenough GM, Johansson ME, Gustafsson JK, Bergstrom JH, Hansson GC (2015) New developments in goblet cell mucus secretion and function. Mucosal Immunol 8(4):712–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchholz K, Ruthmann A (1995) The mesenchyme-like layer of the fiber cells of Trichoplax adhaerens (Placozoa), a syncytium. Z Naturforsch C Biosci 50c:282–285

  • Caccia S, Casartelli M, Tettamanti G (2019) The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell Tissue Res 377(3):505–525

    Article  CAS  PubMed  Google Scholar 

  • Driscoll T, Gillespie JJ, Nordberg EK, Azad AF, Sobral BW (2013) Bacterial DNA sifted from the Trichoplax adhaerens (Animalia: Placozoa) genome project reveals a putative rickettsial endosymbiont. Genome Biol Evol 5(4):621–645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eitel M, Francis WR, Varoqueaux F, Daraspe J, Osigus HJ, Krebs S, Vargas S, Blum H, Williams GA, Schierwater B, Worheide G (2018) Comparative genomics and the nature of placozoan species. PLoS Biol 16(7):e2005359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eitel M, Guidi L, Hadrys H, Balsamo M, Schierwater B (2011) New insights into placozoan sexual reproduction and development. PLoS ONE 6(5):e19639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eitel M, Osigus HJ, DeSalle R, Schierwater B (2013) Global diversity of the Placozoa. PLoS ONE 8(4):e57131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eitel M, Schierwater B (2010) The phylogeography of the Placozoa suggests a taxon-rich phylum in tropical and subtropical waters. Mol Ecol 19(11):2315–2327

    Article  CAS  PubMed  Google Scholar 

  • Fortunato A, Aktipis A (2019) Social feeding behavior of Trichoplax adhaerens. Front Ecol Evol 7

  • Garbowski Tv (1903) Morphogenetische Studien : als Betrag zur Methodologie zoologischer Forschung

  • Grell KG (1971) Trichoplax adhaerens F.E. Schulze und die Entstehung der Metazoen. Naturwiss Rundschau 24:160–161

    Google Scholar 

  • Grell K (1981) Trichoplax adhaerens and the origin of Metazoa. In: Lincei AdC (ed) Origine dei Grandi Phyla dei Metazoi, , eds. 1981. pp. . Accademia Nazionale dei Lincei, Convegno Intern., pp 101–127

  • Grell KG, Benwitz G (1971) Die Ultrastruktur von Trichoplax adhaerens F. E Schulze Cytobiologie 4:216–240

    Google Scholar 

  • Grell KG, Benwitz G (1974) [Special connecting structures between fiber cells of Trichoplax adhaerens F. E. Schulze (author's transl)]. Z Naturforsch C Biosci 29(11–12):790

  • Grell KG, Benwitz G (1981) Additional investigations on the ultrastructure of Trichoplax adhaerens F.E. Schulze (Placozoa) Zoomorphology 98(1):47–67

  • Grell KG, Ruthmann A (1991) Placozoa. In: Harrison FW (ed) Microscopic anatomy of invertebrates. Wiley-Liss, New York, pp 13–27

    Google Scholar 

  • Gruber-Vodicka HR, Leisch N, Kleiner M, Hinzke T, Liebeke M, McFall-Ngai M, Hadfield MG, Dubilier N (2019) Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2. Nat Microbiol 4(9):1465–1474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guidi L, Eitel M, Cesarini E, Schierwater B, Balsamo M (2011) Ultrastructural analyses support different morphological lineages in the phylum Placozoa Grell, 1971. J Morphol 272(3):371–378

    Article  PubMed  Google Scholar 

  • Heyland A, Croll R, Goodall S, Kranyak J, Wyeth R (2014) Trichoplax adhaerens, an enigmatic basal metazoan with potential. Methods Mol Biol 1128:45–61

    Article  CAS  PubMed  Google Scholar 

  • Jackson AM, Buss LW (2009) Shiny spheres of placozoans (Trichoplax) function in anti-predator defense. Invertebr Biol 128(3):205–212

    Article  Google Scholar 

  • Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K, Schierwater B (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214(4):170–175

    Article  CAS  PubMed  Google Scholar 

  • Kaelberer MM, Bohorquez DV (2018) The now and then of gut-brain signaling. Brain Res 1693(Pt B):192–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamm K, Osigus HJ, Stadler PF, DeSalle R, Schierwater B (2018) Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction. Sci Rep 8(1):11168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kamm K, Osigus HJ, Stadler PF, DeSalle R, Schierwater B (2019) Genome analyses of a placozoan rickettsial endosymbiont show a combination of mutualistic and parasitic traits. Sci Rep 9(1):17561

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klinges JG, Rosales SM, McMinds R, Shaver EC, Shantz AA, Peters EC, Eitel M, Worheide G, Sharp KH, Burkepile DE, Silliman BR, Vega Thurber RL (2019) Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov. ISME J 13(12):2938–2953

  • Knoop KA, Newberry RD (2018) Goblet cells: multifaceted players in immunity at mucosal surfaces. Mucosal Immunol 11(6):1551–1557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laumer CE, Gruber-Vodicka H, Hadfield MG, Pearse VB, Riesgo A, Marioni JC, Giribet G (2018) Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias. Elife 7

  • Ma J, Rubin BK, Voynow JA (2018) Mucins, mucus, and goblet cells. Chest 154(1):169–176

    Article  PubMed  Google Scholar 

  • Mayorova TD, Hammar K, Winters CA, Reese TS, Smith CL (2019) The ventral epithelium of Trichoplax adhaerens deploys in distinct patterns cells that secrete digestive enzymes, mucus or diverse neuropeptides. Biol Open 8(8)

  • Mayorova TD, Smith CL, Hammar K, Winters CA, Pivovarova NB, Aronova MA, Leapman RD, Reese TS (2018) Cells containing aragonite crystals mediate responses to gravity in Trichoplax adhaerens (Placozoa), an animal lacking neurons and synapses. PLoS ONE 13(1):e0190905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miyazawa H, Osigus HJ, Rolfes S, Kamm K, Schierwater B, Nakano H (2020) Mitochondrial genome evolution of placozoans: gene rearrangements and repeat expansions. Genome Biol Evol

  • Miyazawa H, Yoshida MA, Tsuneki K, Furuya H (2012) Mitochondrial genome of a Japanese placozoan. Zoolog Sci 29(4):223–228

    Article  CAS  PubMed  Google Scholar 

  • Moroz LL (2018) Neurosystematics and periodic system of neurons: model vs reference species at single-cell resolution. ACS Chem Neurosci 9(8):1884–1903

    Article  CAS  PubMed  Google Scholar 

  • Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, Buckley KM, Ptitsyn A, Reshetov D, Mukherjee K, Moroz TP, Bobkova Y, Yu F, Kapitonov VV, Jurka J, Bobkov YV, Swore JJ, Girardo DO, Fodor A, Gusev F, Sanford R, Bruders R, Kittler E, Mills CE, Rast JP, Derelle R, Solovyev VV, Kondrashov FA, Swalla BJ, Sweedler JV, Rogaev EI, Halanych KM, Kohn AB (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510(7503):109–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moroz LL, Romanova DY, Kohn AB (2021) Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters. Phil Trans R Soc B 376 (1821):20190762; https://doi.org/10.1098/rstb.2019.0762

  • Moroz LL, Romanova DY, Nikitin MA, Sohn D, Kohn AB, Neveu E, Varoqueaux F, Fasshauer D (2020a) The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission. Sci Rep 10(1):13020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moroz LL, Sohn D, Romanova DY, Kohn AB (2020b) Microchemical identification of enantiomers in early-branching animals: lineage-specific diversification in the usage of D-glutamate and D-aspartate. Biochem Biophys Res Commun 527(4):947–952

    Article  CAS  PubMed  Google Scholar 

  • Nielsen C (2019) Early animal evolution: a morphologist’s view. R Soc Open Sci 6(7):190638

    Article  PubMed  PubMed Central  Google Scholar 

  • Nikitin M (2015) Bioinformatic prediction of Trichoplax adhaerens regulatory peptides. Gen Comp Endocrinol 212:145–155

    Article  CAS  PubMed  Google Scholar 

  • Osigus HJ, Rolfes S, Herzog R, Kamm K, Schierwater B (2019) Polyplacotoma mediterranea is a new ramified placozoan species. Curr Biol 29(5):R148–R149

    Article  CAS  PubMed  Google Scholar 

  • Pearse VB, Uehara T, Miller RL (1994) Birefringent granules in placozoans (Trichoplax adhaerens). Trans Am Microsc Soc 113:385–389

    Article  Google Scholar 

  • Pereira RT, Nebo C, de Paula NL, Fortes-Silva R, Cardoso R, de Oliveira I, Paulino RR, Drummond CD, Rosa PV (2020) Distribution of goblet and endocrine cells in the intestine: a comparative study in Amazonian freshwater Tambaqui and hybrid catfish. J Morphol 281(1):55–67

    Article  PubMed  Google Scholar 

  • Rassat J, Ruthmann A (1979) Trichoplax adhaerens F.E. Schulze (Placozoa) in the scanning electron microscope. Zoomorphologie 72:59–72

    Article  Google Scholar 

  • Romanova DY (2019) Cell types diversity of H4 haplotype Placozoa sp. Marine Biological Journal 4(1):81–90

    Article  Google Scholar 

  • Romanova DY, Heyland A, Sohn D, Kohn AB, Fasshauer D, Varoqueaux F, Moroz LL (2020a) Glycine as a signaling molecule and chemoattractant in Trichoplax (Placozoa): insights into the early evolution of neurotransmitters. NeuroReport 31(6):490–497

    Article  CAS  PubMed  Google Scholar 

  • Romanova DY, Smirnov IV, Nikitin MA, Kohn AB, Borman AI, Malyshev AY, Balaban PM, Moroz LL (2020b) Sodium action potentials in placozoa: insights into behavioral integration and evolution of nerveless animals. Biochem Biophys Res Commun 532(1):120–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruthmann A, Behrendt G, Wahl R (1986) The ventral epithelium of Trichoplax adhaerens (Placozoa): Cytoskeletal structures, cell contacts and endocytosis. Zoomorphology 106:115–122

    Article  Google Scholar 

  • Schierwater B, DeSalle R (2018) Placozoa. Curr Biol 28(3):R97–R98

    Article  CAS  PubMed  Google Scholar 

  • Schulze FE (1883) Trichoplax adhaerens, nov. gen., nov. spec. Zool Anz 6:92–97

    Google Scholar 

  • Schulze FE (1891) Uber Trichoplax adhaerens Phys Abh Kgl Acad Wiss Berl,:1–23

  • Schwartz V (1984) Das radialpolare Differenzierungsmuster bei Trichoplax adhaerens F. E. Schulze (Placozoa) [The Radial Polar Pattern of Differentiation in Trichoplax adhaerens F. E. Schulze (Placozoa)]. Z Naturforsch, B J Chem Sci 39c:818–832

  • Sebe-Pedros A, Chomsky E, Pang K, Lara-Astiaso D, Gaiti F, Mukamel Z, Amit I, Hejnol A, Degnan BM, Tanay A (2018) Early metazoan cell type diversity and the evolution of multicellular gene regulation. Nat Ecol Evol 2(7):1176–1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Senatore A, Reese TS, Smith CL (2017) Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses. J Exp Biol 220(Pt 18):3381–3390

    Article  PubMed  PubMed Central  Google Scholar 

  • Signorovitch AY, Dellaporta SL, Buss LW (2006) Caribbean placozoan phylogeography. Biol Bull 211(2):149–156

    Article  PubMed  Google Scholar 

  • Smith CL, Mayorova TD (2019) Insights into the evolution of digestive systems from studies of Trichoplax adhaerens. Cell Tissue Res 377(3):353–367

    Article  PubMed  Google Scholar 

  • Smith CL, Pivovarova N, Reese TS (2015) Coordinated feeding behavior in Trichoplax, an animal without synapses. PLoS ONE 10(9):e0136098

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith CL, Reese TS (2016) Adherens junctions modulate diffusion between epithelial cells in Trichoplax adhaerens. Biol Bull 231(3):216–224

    Article  CAS  PubMed  Google Scholar 

  • Smith CL, Reese TS, Govezensky T, Barrio RA (2019) Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system. Proc Natl Acad Sci U S A 116(18):8901–8908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith CL, Varoqueaux F, Kittelmann M, Azzam RN, Cooper B, Winters CA, Eitel M, Fasshauer D, Reese TS (2014) Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan Trichoplax adhaerens. Curr Biol 24(14):1565–1572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Specian RD, Oliver MG (1991) Functional biology of intestinal goblet cells. Am J Physiol 260(2 Pt 1):C183-193

    Article  CAS  PubMed  Google Scholar 

  • Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454(7207):955–960

    Article  CAS  PubMed  Google Scholar 

  • Starunov VV (2019) The organization of musculature and the nervous system in the pygidial region of phyllodocid annelids. Zoomorphology 138(1):55–71

    Article  Google Scholar 

  • Syed T, Schierwater B (2002) Trichoplax adhaerens: Discovered as a missing link, forgotten as a hydrozoan, re-discovered as a key to metazoan evolution. Vie Milieu 52:177–187

    Google Scholar 

  • Thiemann M, Ruthmann A (1990) Zoomorphology spherical forms of Trichoplax adhaerens (Placozoa). Zoomorphology 110(1):37–45

    Article  Google Scholar 

  • Varoqueaux F, Fasshauer D (2017) Getting nervous: An Evolutionary overhaul for communication. Annu Rev Genet 51:455–476

    Article  CAS  PubMed  Google Scholar 

  • Varoqueaux F, Williams EA, Grandemange S, Truscello L, Kamm K, Schierwater B, Jekely G, Fasshauer D (2018) High cell diversity and complex peptidergic signaling Underlie placozoan behavior. Curr Biol 28(21):3495–3501 e3492

  • Voigt O, Collins AG, Pearse VB, Pearse JS, Ender A, Hadrys H, Schierwater B (2004) Placozoa—no longer a phylum of one. Curr Biol 14(22):R944-945

    Article  CAS  PubMed  Google Scholar 

  • Wenderoth H (1986) Transepithelial cytophagy by Trichoplax adhaerens F.E. Schulze (Placozoa) feeding on yeast. Z Naturforsch, B J Chem Sci 41c:343–347

  • Wenderoth H (1994) Phycoerythrin: Release from cryptophycean algae and bilin storage by the primitive metazoon Trichoplax adhaerens (Placozoa) Zeitschrift für Naturforschung 49c(7–8):458–463

  • Whelan NV, Kocot KM, Moroz TP, Mukherjee K, Williams P, Paulay G, Moroz LL, Halanych KM (2017) Ctenophore relationships and their placement as the sister group to all other animals. Nat Ecol Evol 1(11):1737–1746

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuccolotto-Arellano J, Cuervo-Gonzalez R (2020) Binary fission in Trichoplax is orthogonal to the subsequent division plane. Mech Dev 162:103608

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank E. Bedoshvili, A. Miroliubov, and V. Starunov for their help in electron microscopy, sample preparation, and advice for SEM protocols.

Funding

This work was supported by the Human Frontiers Science Program (RGP0060/2017) and National Science Foundation (1146575, 1557923, 1548121, and 1645219) grants to L.L.M., Russian Ministry of Science and High Education (agreement 075-15-2020-801) grant to D.R., and the Swiss National Science Foundation (#31003A_182732) grant to D.F. The research reported in this publication was also supported in part by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award Number R01NS114491 (to L.L.M.). M. Eitel received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement no 764840.

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D.Y.R., F.V., D.F., and L.L.M. designed the study; D.Y.R., F.V., J.D., M.A.N., M.E., and L.L.M analyzed the data; D.Y.R., L.L.M, F.V., and D.F. wrote the paper; and all authors reviewed, commented on, and edited the manuscript.

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Correspondence to Daria Y. Romanova, Dirk Fasshauer or Leonid L. Moroz.

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Romanova, D.Y., Varoqueaux, F., Daraspe, J. et al. Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis. Cell Tissue Res 385, 623–637 (2021). https://doi.org/10.1007/s00441-021-03459-y

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