SALMFamide2 and serotonin immunoreactivity in the nervous system of some acoels (<scp>X</scp>enacoelomorpha)

Dittmann, Isabel L.; Zauchner, Thomas; Nevard, Lucy; Telford, Maximilian J.; Egger, Bernhard

doi:10.1002/jmor.20794

Cited by 12 publications

(12 citation statements)

References 37 publications

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“…It has been reported that two different antibodies that were raised against echinoderm SALMFamides show immunoreactivity in xenacoelomorphs [49, 51]. While one SALMFamide antibody showed cross-reactivity in different deuterostome and protostome taxa, another one only stained nerves in ambulacrarians, X. bocki and three acoel species [49, 51]. These similarities would be in line with the previous notion of an affinity of Xenacoelomorpha to ambulacrarians [30].…”

Section: Discussionsupporting

confidence: 82%

“…Several acoel LxFamide that share the SxLHFamide motif and some of the SSxxxFamide peptides show sequence similarity to L-type SALMFamides (Figures 13, 14 and 18) that are so far only known from echinoderms [99-101]. It has been reported that two different antibodies that were raised against echinoderm SALMFamides show immunoreactivity in xenacoelomorphs [49, 51]. While one SALMFamide antibody showed cross-reactivity in different deuterostome and protostome taxa, another one only stained nerves in ambulacrarians, X. bocki and three acoel species [49, 51].…”

Section: Discussionmentioning

confidence: 99%

“…Brains and nerve cords can only be found in acoelomorphs, and the ones that are present in extant species do not seem to be homologous to the brains and nerve cords of protostomes or deuterostomes [40, 42, 110]. The brain-like condensations and 1-2 pairs of nerve cords in nemertodermatids are usually situated in a basiepidermal position, which is presumed to be ancestral, whereas the acoel nervous system is often considered to be more derived, and their brains and 2-4 pairs of nerve cords are usually internalized in the body [36-40, 42, 46, 51, 111]. Nemertodermatids as well as acoels possess a variety of clade-specific and species-specific multi-copy peptides, which indicates a stronger subsequent diversification of neuropeptide signaling within Acoelomorpha, Nemertodermatida and Acoela.…”

Section: Discussionmentioning

confidence: 99%

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Changes in the neuropeptide complement correlate with nervous system architectures in xenacoelomorphs

Thiel

Franz‐Wachtel

Aguilera

et al. 2018

Preprint

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Neuropeptides are essential neurosecretory signaling molecules common in protostomes and deuterostomes (together Nephrozoa). Not much, however, is known about the neuropeptide complement of the sister group Xenacoelomorpha. This group is comprised of the three clades Xenoturbella, Nemertodermatida, and Acoela, which differ strongly in their nervous system anatomy. In order to reconstruct the ancestral bilaterian neuropeptide complement and gain insights into neuropeptide evolution within Xenacoelomorpha, we analyzed transcriptomes of 13 acoels, nemertodermatids, and Xenoturbella species. Together with motif searches, similarity searches, mass spectrometry and phylogenetic analyses of neuropeptide precursors and neuropeptide receptors, we reconstruct the xenacoelomorph neuropeptide complement. Our comparison of xenacoelomorph GPCRs with cnidarian and nephrozoan neuropeptide receptors shows that the neuropeptide signaling diversified into at least 20 ancestral peptidergic systems in the lineage to Bilateria. We find that Xenoturbella species possess many of the ancestral bilaterian peptidergic systems and only a few clade-specific neuropeptides. Nemertodermatids seem to have nearly the complete complement of ancestral bilaterian systems and several novel neuropeptides. Acoels show an extensive loss of conserved bilaterian systems, but gained the highest number of novel and group-specific neuropeptides. While it is difficult to correlate the emergence of the bilaterian neuropeptide complement with the evolution of centralized nervous systems, we find a correlation between nervous system novelties and the expansion of taxon-specific neuropeptides in Xenacoelomorpha. References1 Mirabeau, O., Joly, J. S. 2013 Molecular evolution of peptidergic signaling systems in bilaterians. Proc GPCR Network: a large-scale collaboration to determine human GPCR structure and function. Nat Rev (ghrelin, obestatin and nesfatin-1) levels in serum and reproductive tissues of female and male rats with fructose-induced metabolic syndrome. Neuropeptides. 48, 167-177.

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Section: Discussionsupporting

confidence: 82%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Changes in the neuropeptide complement correlate with nervous system architectures in xenacoelomorphs

Thiel

Franz‐Wachtel

Aguilera

et al. 2018

Preprint

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“…Of note, and highly relevant as an experimental system, is their ability to regenerate a full brain from scratch. This is a rather unique feature and allows researchers to follow the regeneration process of a brain with remarkable detail . Planarians and acoelomorphs have distinctive totipotent stem cells (neoblasts) responsible for the renewal of all cell types during development, growth, and regeneration .…”

Section: Symsagittifera Roscoffensis As An Emerging Marine System To mentioning

confidence: 99%

An Emerging System to Study Photosymbiosis, Brain Regeneration, Chronobiology, and Behavior: The Marine Acoel Symsagittifera roscoffensis

et al. 2018

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The acoel worm Symsagittifera roscoffensis, an early offshoot of the Bilateria and the only well-studied marine acoel that lives in a photosymbiotic relationship, exhibits a centralized nervous system, brain regeneration, and a wide repertoire of complex behaviors such as circatidal rhythmicity, photo/geotaxis, and social interactions. While this animal can be collected by the thousands and is studied historically, significant progress is made over the last decade to develop it as an emerging marine model. The authors here present the feasibility of culturing it in the laboratory and describe the progress made on different areas, including genomic and tissue architectures, highlighting the associated challenges. In light of these developments, and on the ability to access abundant synchronized embryos, the authors put forward S. roscoffensis as a marine system to revisit questions in the areas of photosymbiosis, regeneration, chronobiology, and the study of complex behaviors from a molecular and evolutionary perspective.

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“…2005 ; Kotikova and Raiikova 2008 ; Semmler et al. 2010 ; Achatz and Martinez 2012 ; Børve and Hejnol 2014 ; Dittmann et al. 2018 ).…”

Section: Introductionunclassified

Xenacoelomorph Neuropeptidomes Reveal a Major Expansion of Neuropeptide Systems during Early Bilaterian Evolution

Thiel

Franz‐Wachtel

Aguilera

et al. 2018

Molecular Biology and Evolution

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Neuropeptides are neurosecretory signaling molecules in protostomes and deuterostomes (together Nephrozoa). Little, however, is known about the neuropeptide complement of the sister group of Nephrozoa, the Xenacoelomorpha, which together form the Bilateria. Because members of the xenacoelomorph clades Xenoturbella, Nemertodermatida, and Acoela differ extensively in their central nervous system anatomy, the reconstruction of the xenacoelomorph and bilaterian neuropeptide complements may provide insights into the relationship between nervous system evolution and peptidergic signaling. Here, we analyzed transcriptomes of seven acoels, four nemertodermatids, and two Xenoturbella species using motif searches, similarity searches, mass spectrometry and phylogenetic analyses to characterize neuropeptide precursors and neuropeptide receptors. Our comparison of these repertoires with previously reported nephrozoan and cnidarian sequences shows that the majority of annotated neuropeptide GPCRs in cnidarians are not orthologs of specific bilaterian neuropeptide receptors, which suggests that most of the bilaterian neuropeptide systems evolved after the cnidarian–bilaterian evolutionary split. This expansion of more than 20 peptidergic systems in the stem leading to the Bilateria predates the evolution of complex nephrozoan organs and nervous system architectures. From this ancient set of neuropeptides, acoels show frequent losses that correlate with their divergent central nervous system anatomy. We furthermore detected the emergence of novel neuropeptides in xenacoelomorphs and their expansion along the nemertodermatid and acoel lineages, the two clades that evolved nervous system condensations. Together, our study provides fundamental insights into the early evolution of the bilaterian peptidergic systems, which will guide future functional and comparative studies of bilaterian nervous systems.

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SALMFamide2 and serotonin immunoreactivity in the nervous system of some acoels (Xenacoelomorpha)

Cited by 12 publications

References 37 publications

Changes in the neuropeptide complement correlate with nervous system architectures in xenacoelomorphs

Changes in the neuropeptide complement correlate with nervous system architectures in xenacoelomorphs

An Emerging System to Study Photosymbiosis, Brain Regeneration, Chronobiology, and Behavior: The Marine Acoel Symsagittifera roscoffensis

Xenacoelomorph Neuropeptidomes Reveal a Major Expansion of Neuropeptide Systems during Early Bilaterian Evolution

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