A Survey on the Distribution of Ovothiol and ovoA Gene Expression in Different Tissues and Cells: A Comparative Analysis in Sea Urchins and Mussels

Abstract

Ovothiols are histidine-derived thiols produced by a variety of marine invertebrates, protists and bacteria. These compounds, which are among the strongest natural antioxidants, are involved in controlling the cellular redox balance due to their redox exchange with glutathione. Although ovothiols were initially reported as protective agents against environmental stressors, new evidence suggests that they can also act as pheromones and participate in fundamental biological processes such as embryogenesis. To get further insight into the biological roles of ovothiols, we compared ovothiol biosynthesis in the sea urchin Paracentrotus lividus and in the mussel Mytilus galloprovincialis, the two species that represent the richest sources of these compounds among marine invertebrates. Ovothiol content was measured in different tissues and in the immune cells from both species and the expression levels of ovoA, the gene responsible for ovothiol biosynthesis, was inferred from publicly available transcriptomes. A comparative analysis of ovothiol biosynthesis in the two species allowed the identification of the tissues and cells synthesizing the metabolite and highlighted analogies and differences between sea urchins and mussels. By improving our knowledge on the biological roles of ovothiols and pointing out the existence of sustainable natural sources for their isolation, this study provides the basis for future biotechnological investigations on these valuable compounds.

Toxicological Impacts of Microplastics: Effects on Levels of Cellular Thiols in Mytilus galloprovincialis

“…The same trend was recorded in our study, in which we observed that the mantle of female specimens during the breeding season exhibits the highest levels of OSH and GSH after exposure to both low and high micro‐PS concentrations, immediately followed by the gonads. Most likely, this is because eggs are a fundamental source of OSH, positively influencing OSH levels in gonads and in mantle (Murano et al, 2022).…”

“…Evaluation of OA and GSH content was performed by reversed-phase-high-performance liquid chromatography through analysis of their 4-bromomethyl methoxycoumarin (BMC) derivatives, following the procedure already described in Murano et al, 2022. In brief, samples (10 mg) of pooled all male or all female lyophilized mussel tissues from at least four specimens with a maximum of five for both male and female were mixed with 90 µl of lysis buffer (0.75 M HClO 4 :AcCN 2:1) and spiked with 10 µl of 1 mM N-acetyl-cysteine as internal standard. After extensive vortexing, the insoluble tissue debris was removed by centrifugation (5 min, 16 000g), and 15 µl of 2 M K 2 CO 3 were added to 100 µl of supernatant to promote KClO 4 precipitation.…”

“…On the other hand, recent studies have demonstrated that ovothiol A (OSH), a thio‐amino acid originally identified in the eggs of Paracentrotus lividus , is also an essential and abundant cellular thiol in M. galloprovincialis and participates in the response to environmental contaminants (Diaz de Cerio et al, 2020; Murano et al, 2022). Ovothiol A is endowed with unique chemical and redox properties, which mostly derive from the marked acidic character (low acid dissociation constant [p K a ]) of the thiol group, due to its position on the imidazole ring of histidine (Palumbo et al, 2018).…”

The first genetic engineered system for ovothiol biosynthesis in diatoms reveals a mitochondrial localization for the sulfoxide synthase OvoA

“…Indeed, protein localization in the subcellular compartment may offer insightful suggestions on the OvoA biological function, which is far from being completely understood, particularly in diatoms, where the metabolite was only recently identified [16]. Thanks to their ability to scavenge peroxides and participate to redox exchange with GSH, ovothiols have been proposed to protect eggs and early embryos against the oxidative burst occurring at fertilization and during development in sea urchins [38,51], to be involved in the maturation and differentiation of sea urchins female gonads [52], to protect against the oxidative stress produced by the immune response of the host in Trypanosoma species [53], and against environmental pollutants in sea urchins and Mytilus galloprovincialis [26,54]. Therefore, the mitochondrial localization of the OvoA enzyme in diatoms represents a very interesting finding in light of the unique redox properties of ovothiol.…”

Glutathione Depletion Disrupts Redox Homeostasis in an Anoxia-Tolerant Invertebrate

“…These findings suggest a potential role of ascorbate and uric acid in anoxia/hypoxia tolerance in gastropods. Moreover, although ovothiols have not yet been determined in land snails, they are present in high concentrations in the organs of mussels [ 81 ] and other aquatic mollusks [ 82 ], indicating their potential relevance for redox control under anoxia/hypoxia stress. Therefore, evidence from other experimental systems suggests that these antioxidant molecules and their potential role in the POS mechanism should be investigated in H. aspersa and other animal models in further research.…”