Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism

Abstract

Ocean acidification (OA) refers to the decrease in ocean water pH resulting from the increasing absorption of atmospheric CO 2. This will cause changes in the ocean's carbonate chemistry system with a resulting impact on reproduction of marine organisms. Reproduction is the fundamental process that allows the conservation of the species; in free-spawning marine invertebrates, this process is highly sensitive to changes in seawater quality and chemistry. To date, the majority of the studies concerned OA effects on reproduction has been focused on embryo and larval development. Despite several evidence for the impairment of reproductive success by environmental perturbations through altering gamete quality, sperm physiological responses to OA are poorly investigated. In this study, we evaluated the effects of exposure to acidified seawater (AcSW) (pH 7.8), which approximate the predicted global averages for oceanic surface waters at the end of this century, on sperm quality of the mussel Mytilus galloprovincialis and the ascidian Ciona robusta by evaluating several endpoints, such as motility, vitality, mitochondrial activity, oxidative state, and intracellular pH (pH i). Following sperm exposure to AcSW, the percentage of motile spermatozoa, mitochondrial activity and pH i decreased in comparison to the current seawater pH of 8.1, whereas vitality and oxidative state were unaffected by the low external pH in both the species. In broadcast spawners, a relationship between sperm intracellular pH and the initiation of motility are well known. Spermatozoa are immotile in the testes and motility is induced after the spermatozoa are released into seawater; the alkaline pH of seawater, in fact, increases the pH i activating motility and mitochondrial respiration. The results of this study suggest that the lowering of seawater pH as predicted to occur for 2100, through the inhibition of pH i increase, prevent sperm motility activation. Sperm motility is a key determinant of fertilization success; consequently, a corresponding drop in fertilization success would be expected with important implications for the fitness and the survival of marine invertebrates.

Molecular mechanisms of sperm motility are conserved in an early-branching metazoan

“…It is possible that regulation of mitochondrial output via sAC-PKA signaling in invertebrate sperm is an additional means of “tuning” flagellar motility. Importantly, because mitochondrial function and sperm motility are both impaired under simulated ocean acidification in sea urchin, mussel, and ascidian sperm ( 21 , 67 ), a description of the molecular mechanisms underlying sperm motility and their response to environmental conditions is critical for predicting the susceptibility of reproduction to climate change.…”

“…Sperm in particular are acutely susceptible to environmental disturbances due to their small size and brief lifespan (13), and climate change stressors including ocean warming and acidification have reduced coral sperm production (11,14), motility (10,15,16), and fertilization success (17,18) in several species. The mechanisms driving these declines in sperm performance are unknown, but both warming and acidification may disrupt coral cellular metabolism and acidify the cytosol (19)(20)(21), two processes that are important for sperm motility in other species (22). Indeed, initial evidence indicates that alkalinization of coral sperm cytosol promotes motility (23), highlighting the importance of understanding the Significance Reef-building corals are the keystone species of the world's most biodiverse yet threatened marine ecosystems.…”

Molecular mechanisms of sperm motility are conserved in a basal metazoan

“…Although the influence of sAC activity on sperm mitochondrial function remains unexplored, it is possible that regulation of mitochondrial output via sAC is an additional means of "tuning" flagellar motility. Importantly, because mitochondrial function and sperm motility are both impaired under simulated ocean acidification in sea urchin, mussel, and ascidian sperm (21,61), a description of the molecular mechanisms underlying sperm motility and their response to environmental conditions are critical for predicting the susceptibility of reproduction to climate change.…”

“…Sperm, in particular, are an acutely susceptible life stage to environmental disturbances due to their small size and brief life span (13), and climate change stressors including ocean warming and acidification have reduced coral sperm production (11,14), motility (10,15,16) and fertilization success (17,18). The mechanisms driving these declines in sperm performance are unknown, but both warming and acidification may disrupt coral cellular metabolism and acidify the cytosol (19)(20)(21), two processes that are important for sperm motility in other species (22). Indeed, initial evidence indicates that alkalinization of coral sperm cytosol promotes motility (23), highlighting the importance of understanding the molecular pathways that connect pH-dependent signaling with changes in cellular performance.…”

Ocean Acidification, but Not Environmental Contaminants, Affects Fertilization Success and Sperm Motility in the Sea Urchin Paracentrotus lividus

“…On the contrary, the effects of OA in combination with aquatic pollutants on gametes are still poorly studied. Nonetheless, it was observed that significant and persistent changes in environmental variables, such as pH, might affect the normal reproductive success of different marine species including bivalves [31][32][33], sea urchins [34][35][36][37][38], corals [39][40][41], polychaetes [28,42], and also fish [43]. Marine broadcast spawners, such as echinoderms, might be particularly susceptible to OA and pollutants because of their reproductive strategy.…”