Nitric oxide signaling in ctenophores

Abstract

Nitric oxide (NO) is one of the most ancient and versatile signal molecules across all domains of life. NO signaling might also play an essential role in the origin of animal organization. Yet, practically nothing is known about the distribution and functions of NO-dependent signaling pathways in representatives of early branching metazoans such as Ctenophora. Here, we explore the presence and organization of NO signaling components using Mnemiopsis and kin as essential reference species. We show that NO synthase (NOS) is present in at least eight ctenophore species, including Euplokamis and Coeloplana, representing the most basal ctenophore lineages. However, NOS could be secondarily lost in many other ctenophores, including Pleurobrachia and Beroe. In Mnemiopsis leidyi, NOS is present both in adult tissues and differentially expressed in later embryonic stages suggesting the involvement of NO in developmental mechanisms. Ctenophores also possess soluble guanylyl cyclases as potential NO receptors with weak but differential expression across tissues. Combined, these data indicate that the canonical NO-cGMP signaling pathways existed in the common ancestor of animals and could be involved in the control of morphogenesis, cilia activities, feeding and different behaviors.

Neuronal gene expression in two generations of the marine parasitic worm, Cryptocotyle lingua

“…We propose that the loss of nitric oxide synthase in Platyhelminthes was compensated by the peculiarities of the parasitic lifestyle of these animals, which allows for unrestricted use of host-derived NO. Similar losses of the gene for this enzyme were reported for representatives of Ctenophora 64 and for nematodes in which it has been attributed to consequences of life in an environment enriched with nitric oxide by bacteria 65 . However, the lack of NOS in trematodes does not mean the absence of the NO signaling pathway.…”

Nitric oxide suppresses cilia activity in ctenophores

“…However, NOS was detected in basal and more derived species of ctenophores, such as Mnemiopsis leidyi (Moroz and Kohn, 2016;Moroz et al, 2020a) and Bolinopsis (Moroz et al, 2023). These comparative analyses illustrate the mosaic nature of NOS distribution within the phylum Ctenophora and provide evidence for the secondary loss of NOS in Pleurobrachia from the common ancestor of ctenophores (Moroz et al, 2023). However, Pleurobrachia has soluble guanylyl cyclases and possibly other receptors for NO, which might sense this molecule from alternative endogenous and exogenous sources (e.g., microbiomes and/or food).…”

“…Nitric oxide (NO) is an ancient and versatile signal molecule (Moroz and Kohn, 2011a), recently proposed as a transmitter candidate in ctenophores (Moroz and Kohn, 2016;Moroz et al, 2023). In contrast to classical transmitters, the application NO donors (NOC-9 and Diethylamine NONOate, 0.02-0.2 mM) caused inhibition of comb cilia beating both in Pleurobrachia and Bolinopsis with a complete arrest of cilia activity in most cases at higher concentrations, >70-100 µm (Figure 7).…”

Multiple parallel expansions of bilaterian-like phototransduction gene families in the eyeless Anthozoa

“…The N. vectensis candidate protein sequences were also searched in the genome assemblies of Alatina alata (Ohdera et al, 2019) and Aurelia aurita (Gold et al, 2019), and the top query hits were saved. Additional sequences were obtained from alignments from (Krishnan et al, 2015; Lagman et al, 2022; Moroz et al, 2023; Peng et al, 2015; Vöcking et al, 2022) and redundant sequences were not included.…”