The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission

Moroz, Leonid L.; Romanova, Daria Y.; Никитин, М. А.; Sohn, Dosung; Kohn, Andrea B.; Neveu, Émilie; Varoqueaux, Frédérique; Fasshauer, Dirk

doi:10.1038/s41598-020-69851-w

Cited by 45 publications

(44 citation statements)

References 102 publications

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“…These NIT domains were previously characterized in prokaryotes (e.g., bacteria and cyanobacteria) (33). This unusual molecular architecture implies the existence in animals of previously unidentified nitrite or nitrate sensing (34), which might have broad implications for environmental biology. NO and products of NO oxidation might also contribute to innate immunity and be a part of the nitrogen cycle in the marine environment.…”

Section: Neural Signaling Complexity and Neuroimmune Interactions In H Americanusmentioning

confidence: 78%

The American lobster genome reveals insights on longevity, neural, and immune adaptations

et al. 2021

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The American lobster, Homarus americanus, is integral to marine ecosystems and supports an important commercial fishery. This iconic species also serves as a valuable model for deciphering neural networks controlling rhythmic motor patterns and olfaction. Here, we report a high-quality draft assembly of the H. americanus genome with 25,284 predicted gene models. Analysis of the neural gene complement revealed extraordinary development of the chemosensory machinery, including a profound diversification of ligand-gated ion channels and secretory molecules. The discovery of a novel class of chimeric receptors coupling pattern recognition and neurotransmitter binding suggests a deep integration between the neural and immune systems. A robust repertoire of genes involved in innate immunity, genome stability, cell survival, chemical defense, and cuticle formation represents a diversity of defense mechanisms essential to thrive in the benthic marine environment. Together, these unique evolutionary adaptations contribute to the longevity and ecological success of this long-lived benthic predator.

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Section: Neural Signaling Complexity and Neuroimmune Interactions In H Americanusmentioning

confidence: 78%

The American lobster genome reveals insights on longevity, neural, and immune adaptations

et al. 2021

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“…In contrast with other invertebrates studied, placozoans of genera Trichoplax and Hoilungia have three distinct NOS genes, including a PDZ domain-containing NOS [168]. Distinct NOSs are expressed in different subpopulations of cells, with a noticeable distribution close to the edge regions of Trichoplax.…”

Section: (A) Nitric Oxide and Atpmentioning

confidence: 90%

“…R. Soc. B 376: 20190762 [46,168,171,231]. Of note, the predicted PAH enzymes in two ctenophores, Pleurobrachia and Mnemiopsis, both cluster with the cnidarian PAH enzymes.…”

Section: (F ) Biogenic Aminesmentioning

confidence: 98%

“…Genomes of ctenophores, placozoans and sponges encode purinergic P2X receptors and may use ATP as a signal molecule, but their systemic functional roles are unknown. There is one described truncated NOS gene in two ctenophore species, Mnemiopsis and Cestum, with unknown function [168]. Other studied ctenophores apparently lost NOS.…”

Section: (A) Nitric Oxide and Atpmentioning

confidence: 99%

“…The most surprising discovery was in receptor machinery for NO. It includes both canonical and novel NIT-domain-containing soluble guanylate cyclases as putative NO/nitrite/nitrate sensors [168]. Thus, although Trichoplax and Hoilungia exemplify the morphologically simplest free-living animals, the complexity of NO-cGMPmediated signalling in Placozoa is greater than in vertebrates.…”

Section: (A) Nitric Oxide and Atpmentioning

confidence: 99%

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Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters

Moroz

Romanova

Kohn

2021

Phil. Trans. R. Soc. B

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113

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Transmitter signalling is the universal chemical language of any nervous system, but little is known about its early evolution. Here, we summarize data about the distribution and functions of neurotransmitter systems in basal metazoans as well as outline hypotheses of their origins. We explore the scenario that neurons arose from genetically different populations of secretory cells capable of volume chemical transmission and integration of behaviours without canonical synapses. The closest representation of this primordial organization is currently found in Placozoa, disk-like animals with the simplest known cell composition but complex behaviours. We propose that injury-related signalling was the evolutionary predecessor for integrative functions of early transmitters such as nitric oxide, ATP, protons, glutamate and small peptides. By contrast, acetylcholine, dopamine, noradrenaline, octopamine, serotonin and histamine were recruited as canonical neurotransmitters relatively later in animal evolution, only in bilaterians. Ligand-gated ion channels often preceded the establishment of novel neurotransmitter systems. Moreover, lineage-specific diversification of neurotransmitter receptors occurred in parallel within Cnidaria and several bilaterian lineages, including acoels. In summary, ancestral diversification of secretory signal molecules provides unique chemical microenvironments for behaviour-driven innovations that pave the way to complex brain functions and elementary cognition. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens'.

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The enigmatic Placozoa part 1: Exploring evolutionary controversies and poor ecological knowledge

et al. 2021

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The placozoan Trichoplax adhaerens is a tiny hairy plate and more simply organized than any other living metazoan. After its original description by F.E. Schulze in 1883, it attracted attention as a potential model for the ancestral state of metazoan organization, the “Urmetazoon”. Trichoplax lacks any kind of symmetry, organs, nerve cells, muscle cells, basal lamina, and extracellular matrix. Furthermore, the placozoan genome is the smallest (not secondarily reduced) genome of all metazoan genomes. It harbors a remarkably rich diversity of genes and has been considered the best living surrogate for a metazoan ancestor genome. The phylum Placozoa presently harbors three formally described species, while several dozen “cryptic” species are yet awaiting their description. The phylogenetic position of placozoans has recently become a contested arena for modern phylogenetic analyses and view‐driven claims. Trichoplax offers unique prospects for understanding the minimal requirements of metazoan animal organization and their corresponding malfunctions.

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The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission

Cited by 45 publications

References 102 publications

The American lobster genome reveals insights on longevity, neural, and immune adaptations

The American lobster genome reveals insights on longevity, neural, and immune adaptations

Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters

The enigmatic Placozoa part 1: Exploring evolutionary controversies and poor ecological knowledge

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