Profiling cellular diversity in sponges informs animal cell type and nervous system evolution

Musser, Jacob M.; Schippers, Klaske J.; Nickel, Michael; Mizzon, Giulia; Kohn, Andrea B.; Pape, Constantin; Hammel, Jörg U.; Wolf, Florian; Liu, Cong; Hernández-Plaza, Ana; Achim, Kaia; Schieber, Nicole L.; Francis, Warren R.; Vargas, Roger; Kling, Svenja; Renkert, Maike; Feuda, Roberto; Gáspár, Imre; Burkhardt, Pawel; Bork, Peer; Beck, Martin; Kreshuk, Anna; Wörheide, Gert; Huerta-Cepas, Jaime; Schwab, Yannick; Moroz, Leonid L.; Arendt, Detlev

doi:10.1101/758276

Cited by 42 publications

(65 citation statements)

References 88 publications

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“…Contractile behavior of H. panicea is therefore likely driven by an antagonist system which is based on the interplay between contractile pinacoderm cells, water pressure in the canal system and visco-elastic forces of a collagenous matrix with motile cells in the mesohyl (Elliott and Leys, 2007;Nickel et al, 2011;Hammel and Nickel, 2014). Recent work has further described a novel, yet abundant, choanocyte-related cell type in the mesohyl of a freshwater demosponge (myopeptidocyte) which is likely involved in contraction-expansion of sponges (Musser et al, 2019).…”

Section: Functional Morphology Of Contractile Behaviormentioning

confidence: 99%

“…As indicated by a ∼100-fold difference in the glutamate concentration to induce full contractions in E. muelleri (0.08 mM; Elliott and Leys, 2010) or T. wilhelma (10 mM; Ellwanger et al, 2007), respectively, physiological levels and effects of chemical messengers may vary across sponge species (Ellwanger and Nickel, 2006;Ellwanger et al, 2007;Elliott and Leys, 2010). Coordinated contractile responses of demosponges in part also seem to be regulated through nitric-oxide (NO) signaling (Ellwanger and Nickel, 2006;Elliott and Leys, 2010;Musser et al, 2019), which triggers relaxation of endothelial smooth muscle contraction in vertebrates (Palmer et al, 1987). An improved understanding of contractions in sponges on a cellular level may thus provide some fundamental insights into the evolution of nervous systems and muscle tissue in metazoans.…”

Section: Ecological Role Of Contractions In Spongesmentioning

confidence: 99%

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Contraction-Expansion and the Effects on the Aquiferous System in the Demosponge Halichondria panicea

et al. 2020

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Contractile behavior is common among sponges despite their lack of nerves and muscles. As sessile filter-feeders, sponges rely on water with suspended food particles being pumped through their aquiferous system. During contractions, however, the water flow is being reduced and eventually shut down. Yet, purpose and underlying pathways of contractile behavior have remained largely unclear. Here, we document the external and internal morphology of contracted and expanded single-osculum explants of the demosponge Halichondria panicea. We show that contraction-expansion dynamics can occur spontaneously (in untreated explants) and can be induced by exposure to chemical messengers such as γ-aminobutyric acid (GABA, 1 mM) and L-glutamate (L-Glu, 1 mM), or to inedible ink particles (4 mg L −1). The neurotransmitter GABA triggered similar contraction-expansion dynamics in H. panicea as observed in untreated explants. The effects of GABA-induced contraction-expansion events on the aquiferous system were investigated using scanning electron microscopy (SEM) on cryofractured explants. Our findings suggest that contraction-expansion affects the entire aquiferous system of H. panicea, including osculum, ostia, in-and excurrent canals and apopyles.

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Section: Functional Morphology Of Contractile Behaviormentioning

confidence: 99%

Section: Ecological Role Of Contractions In Spongesmentioning

confidence: 99%

Contraction-Expansion and the Effects on the Aquiferous System in the Demosponge Halichondria panicea

et al. 2020

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“…Using these methods, scientists have already profiled a broad taxonomic range of different animals, classified their cell types, profiled their gene expression patterns, and begun to reconstruct their cell differentiation lineages. Single cell transcriptomics has been already used in very diverse animal groups, including sponges [8,9], cnidarians [10,11], planarians [12][13][14][15][16], nematodes [17,18], arthropods [19][20][21][22], ascidians [23] as well as extensively in vertebrates [24][25][26][27][28][29][30][31].…”

Section: Introductionmentioning

confidence: 99%

ACME dissociation: a versatile cell fixation-dissociation method for single-cell transcriptomics

García-Castro

Kenny

Álvarez‐Campos

et al. 2020

Preprint

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Single-cell sequencing technologies are revolutionizing biology, but are limited by the need to dissociate fresh samples that can only be fixed at later stages. We present ACME (ACetic-MEthanol) dissociation, a cell dissociation approach that fixes cells as they are being dissociated. ACME-dissociated cells have high RNA integrity, can be cryopreserved multiple times, can be sorted by Fluorescence-Activated Cell Sorting (FACS) and are permeable, enabling combinatorial single-cell transcriptomic approaches. As a proof of principle, we have performed SPLiT-seq with ACME cells to obtain around ~34K single cell transcriptomes from two planarian species and identified all previously described cell types in similar proportions. ACME is based on affordable reagents, can be done in most laboratories and even in the field, and thus will accelerate our knowledge of cell types across the tree of life.In its original form, the maceration solution simply consisted of acetic acid and glycerol dissolved in water.Baguñà and Romero added methanol, as it speeds up dissociation [42]. Our protocol uses acetic acid and methanol, together with glycerol, dissolved in water. This solution produces fixed single cells in suspension with high integrity RNAs. Conveniently, we show that ACME-dissociated cells can be cryopreserved using DMSO [43] at different points throughout the process, with little detriment to their recovery and RNA integrity. As a proof of principle, we combined ACME to an optimised version of SPLiT-seq [34], including 4 rounds of barcoding, and were able to profile 33,827 cells from two different planarian species, Schmidtea mediterranea and Dugesia japonica, in a single run. We recover all S. mediterranea cell types from a previous study [13], at comparable proportions, showing that ACME dissociation does not introduce biases in cell type composition. Furthermore, we describe for the first time the single-cell transcriptome of D. japonica, opening the study of cell type evolution in this clade. Thus, in combination with SPLiT-seq or other approaches, ACME dissociation is a robust method to obtain high-quality single-cell transcriptomic data from fixed cells.

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“…This condition might have been further stabilized in the "epithelialized" last common ancestor of the metazoans. From this condition many different structural types of synapses, like the presently described neuroid-choanocyte relationship in a sponge (Musser et al 2019), presynaptic triads and somatic synapses in ctenophores (Hernandez-Nicaise 1968) and "classical" synapses present in most other metazoans might have evolved. In this scenario, the structural co-option of ancestral neurosecretory vesicles and polarized vesicular transport at plasma membrane contact sites might be the key process leading the structural evolution of metazoan synapses.…”

Section: Discussionmentioning

confidence: 85%

Choanoflagellates and the ancestry of neurosecretory vesicles

Gohde

Nauman

Laundon

et al. 2020

Preprint

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Neurosecretory vesicles are highly specialized trafficking organelles important for metazoan cell-cell signalling. Despite the high anatomical and functional diversity of neurons in metazoans, the protein composition of neurosecretory vesicles in bilaterians appears to be similar. This similarity points towards a common evolutionary origin. Moreover, many key neurosecretory vesicle proteins predate the origin of the first neurons and some even the origin of the first animals (metazoans). However, little is known about the molecular toolkit of these vesicles in non-bilaterian metazoans and their closest unicellular relatives, making inferences about the evolutionary origin of neurosecretory vesicles extremely difficult. By comparing 28 proteins of the core neurosecretory vesicle proteome in 13 different species, we demonstrate that most of the proteins are already present in unicellular organisms. Surprisingly, we find that the vesicle residing SNARE protein synaptobrevin is localized to the vesicle-rich apical and basal pole in the choanoflagellate Salpingoeca rosetta. Our 3D vesicle reconstructions reveal that the choanoflagellates Salpingoeca rosetta and Monosiga brevicollis exhibit a polarized and diverse vesicular landscape. This study sheds light on the ancestral molecular machinery of neurosecretory vesicles and provides a framework to understand the origin and evolution of secretory cells, synapses, and neurons.

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Profiling cellular diversity in sponges informs animal cell type and nervous system evolution

Cited by 42 publications

References 88 publications

Contraction-Expansion and the Effects on the Aquiferous System in the Demosponge Halichondria panicea

Contraction-Expansion and the Effects on the Aquiferous System in the Demosponge Halichondria panicea

ACME dissociation: a versatile cell fixation-dissociation method for single-cell transcriptomics

Choanoflagellates and the ancestry of neurosecretory vesicles

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