Distribution and diversity of ROS-generating enzymes across the animal kingdom, with a focus on sponges (Porifera)

Abstract

Background Reactive derivatives of oxygen (reactive oxygen species; ROS) are essential in signalling networks of all aerobic life. Redox signalling, based on cascades of oxidation–reduction reactions, is an evolutionarily ancient mechanism that uses ROS to regulate an array of vital cellular processes. Hydrogen peroxide (H2O2) and superoxide anion (O2•−) are employed as signalling molecules that alter the oxidation state of atoms, inhibiting or activating gene activity. Here, we conduct metazoan-wide comparative genomic assessments of the two enzyme families, superoxide dismutase (SOD) and NADPH oxidases (NOX), that generate H2O2 and/or O2•− in animals. Results Using the genomes of 19 metazoan species representing 10 phyla, we expand significantly on previous surveys of these two ancient enzyme families. We find that the diversity and distribution of both the SOD and NOX enzyme families comprise some conserved members but also vary considerably across phyletic animal lineages. For example, there is substantial NOX gene loss in the ctenophore Mnemiopsis leidyi and divergent SOD isoforms in the bilaterians D. melanogaster and C. elegans. We focus particularly on the sponges (phylum Porifera), a sister group to all other metazoans, from which these enzymes have not previously been described. Within Porifera, we find a unique calcium-regulated NOX, the widespread radiation of an atypical member of CuZnSOD named Rsod, and a novel endoplasmic reticulum MnSOD that is prevalent across aquatic metazoans. Conclusions Considering the precise, spatiotemporal specificity of redox signalling, our findings highlight the value of expanding redox research across a greater diversity of organisms to better understand the functional roles of these ancient enzymes within a universally important signalling mechanism.

Nitric oxide signaling in ctenophores

“…NO, and NOS control metamorphosis and symbiotic relationships in the desmosponge Amphimedon ( Ueda et al, 2016 ; Hewitt and Degnan, 2022 ). There is growing evidence that NO can modulate body contractions and coordinated behaviors in freshwater sponges Ephydatia muelleri ( Elliott and Leys, 2010 ), Spongilla lacustris ( Musser et al, 2021 ), and the marine sponge Tethya wilhelma ( Ellwanger and Nickel, 2006 ).…”

Reactive Oxygen Species Signaling and Oxidative Stress: Transcriptional Regulation and Evolution

“…SOD1 and SOD2 are widely distributed across the metazoans, whereas SOD3 is absent in most sponges, a group of species which occupy a unique phylogenetic position as sister to other animal phyla. Traits unique to sponges have been logically traced back to the divergent evolution from a common ancestor [ 133 ]. A study of the ctenophore Mnemiopsis leidyi demonstrated substantial NOX gene loss with the retention of only NOX5 [ 133 , 134 ].…”

“…Traits unique to sponges have been logically traced back to the divergent evolution from a common ancestor [ 133 ]. A study of the ctenophore Mnemiopsis leidyi demonstrated substantial NOX gene loss with the retention of only NOX5 [ 133 , 134 ]. Ctenophores have been considered the earliest diverging animal lineage which share with bilaterians complex cell types such as neural cells [ 135 ].…”

“…M. leidyi exhibits daily vertical migration in response to high radiation levels, which may affect their cellular redox state. Indeed, a comparatively wide range of Cu/ZnSODs are encoded by M. leidyi , which has been suggested to compensate for the reduction in the diversity of encoded NOX enzymes [ 133 ].…”

Antioxidant enzymes that target hydrogen peroxide are conserved across the animal kingdom, from sponges to mammals

“…Antioxidants can be either non-enzymatic (e.g., vitamins E, C, A, selenium, transferrin, and lactoferrin, ascorbic acid, glutathione, melatonin, carotenoids, flavonoids, proline), or specialised enzymes that vary in subcellular localisation, predominant substrate, and rate of reactivity 7,22,23 . The specialist enzymatic antioxidant families include those that target hydrogen peroxide (H 2 O 2 ), which is the major redox signalling ROS reviewed by 5,24,25 , and those that target superoxide anion radical (O 2•-) for the generation of H 2 O 2 as a product[reviewed by 26,27 .The three major families of antioxidants that target H 2 O 2 are monofunctional catalase (CAT), peroxiredoxin (PRX), and glutathione peroxidase (GPX) (Fig. 1A-C) 28,29,30,31 .…”