An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

Abstract

In many marine invertebrates, larval metamorphosis is induced by environmental cues that activate sensory receptors and signalling pathways. Nitric oxide (NO) is a gaseous signalling molecule that regulates metamorphosis in diverse bilaterians. In most cases NO inhibits or represses this process, although it functions as an activator in some species. Here we demonstrate that NO positively regulates metamorphosis in the poriferan Amphimedon queenslandica. High rates of A. queenslandica metamorphosis normally induced by a coralline alga are inhibited by an inhibitor of nitric oxide synthase (NOS) and by a NO scavenger. Consistent with this, an artificial donor of NO induces metamorphosis even in the absence of the alga. Inhibition of the ERK signalling pathway prevents metamorphosis in concert with, or downstream of, NO signalling; a NO donor cannot override the ERK inhibitor. NOS gene expression is activated late in embryogenesis and in larvae, and is enriched in specific epithelial and subepithelial cell types, including a putative sensory cell, the globular cell; DAF-FM staining supports these cells being primary sources of NO. Together, these results are consistent with NO playing an activating role in induction of A. queenslandica metamorphosis, evidence of its highly conserved regulatory role in metamorphosis throughout the Metazoa.

The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

“…This is consistent with the hypothesis presented in Hadfield et al (2001), which argues that competence is a convergent trait that evolved to minimize vulnerability during settlement/metamorphosis (Hadfield 2000). Additionally, certain signaling pathways, such as Nitric Oxide appear to be employed in both primary and secondary metamorphic events, reinforcing convergence (Bishop and Brandhorst 2003, Comes et al 2007, Bishop et al 2008, Ueda and Degnan 2013, Ueda et al 2016. Alternatively, as hypothesized in the reacquisition of planktotrophic larvae (Collin and Miglietta 2008), these similarities may have also been preserved from ancient (and previously lost) life cycles through intact pleiotropic developmental pathways.…”

“…This is not so surprising given the promiscuity and versatility of TFs in various developmental roles within a single species (Cheatle Jarvela and Hinman 2015). However, in light of other similarities between ascidian and ciliated larvae (Hadfield 2000, Ueda and Degnan 2013, Ueda et al 2016, it is also possible that these transcription factors are still indicators of common regulatory ancestry. Given this uncertainty, I created temporal coexpression networks (TCNs) in Amphimedon and Strongylocentrotus to examine expression profiles between species as well as infer regulatory function from suites of coexpressed genes.…”

“…Oxide signaling pathways to initiate metamorphosis (Ueda et al 2016). This suggests that the apical region (posterior region in sponges) in ciliated primary larva across the Metazoa might be involved in environmental sensing.…”

“…Even without neurons, the anterior region of the sponge is capable of distinguishing changes in light intensity (Leys and Degnan 2001), and is suggested to be important to larval settlement , Ueda et al 2016. Specifically, flask cells in the anterior region of the A. queenslandica larvae have been shown to respond to environmental cues via calcium mediated signaling pathways , which in turn interact with Nitric…”

“…KEGG pathway analysis highlights multiple important signaling pathways, including MAPK, Wnt, Notch, Hedgehog, and TGFB, all of which have been experimentally characterized in A. queenslandica. First, MAPK pathways are activated by Nitric Oxide (NO) signaling, playing a positive regulatory role in the induction of A. queenslandica metamorphosis (Ueda et al 2016). Second, Wnt and TGFB expression appears in early cleavage, before migrating to the posterior pole of the developing embryo, and later plays an important role during late embryogenesis and larval development, particularly in the formation of the sensory pigment ring (Adamska et al 2007a(Adamska et al , 2010.…”