High potassium seawater inhibits ascidian sperm chemotaxis, but does not affect the male gamete chemotaxis of a brown alga

• Published in: Zygote (Cambridge) 2019-08, Vol.27 (4), p.225-231
• Main Authors: Kinoshita-Terauchi, Nana, Shiba, Kogiku, Terauchi, Makoto, Romero, Francisco, Ramírez-Gómez, Héctor Vincente, Yoshida, Manabu, Motomura, Taizo, Kawai, Hiroshi, Nishigaki, Takuya
• Format: Article
• Language: English
• Subjects: Algae; Animals; Attractants; Channels; Chemical analysis; Chemotactic factors; Chemotaxis; Chemotaxis - drug effects; Chemotaxis - physiology; Ciona intestinalis - physiology; Efflux; Eukaryotes; Experiments; Female; Gametes; Germ Cells - physiology; Homology; Invertebrates; Male; Marine invertebrates; Motility; Nucleotides; Phaeophyceae; Phaeophyceae - physiology; Potassium; Potassium - chemistry; Potassium - pharmacology; Potassium channels (voltage-gated); Reproduction (biology); Reproduction - drug effects; Reproduction - physiology; Seawater; Seawater - chemistry; Sexual reproduction; Signal Transduction - drug effects; Signaling; Sperm; Spermatozoa - physiology; Sterols; Structural analysis; Water analysis
• ISSN: 0967-1994; 1469-8730
• DOI: 10.1017/S0967199419000224

Male gamete chemotaxis towards the female gamete is a general strategy to facilitate the sexual reproduction in many marine eukaryotes. Biochemical studies of chemoattractants for male gametes of brown algae have advanced in the 1970s and 1980s, but the molecular mechanism of male gamete responses to the attractants remains elusive. In sea urchin, a K+ channel called the tetraKCNG channel plays a fundamental role in sperm chemotaxis and inhibition of K+ efflux through this channel by high K+ seawater blocks almost all cell responses to the chemoattractant. This signalling mechanism could be conserved in marine invertebrates as tetraKCNG channels are conserved in the marine invertebrates that exhibit sperm chemotaxis. We confirmed that high K+ seawater also inhibited sperm chemotaxis in ascidian, Ciona intestinalis (robusta), in this study. Conversely, the male gamete chemotaxis towards the female gamete of a brown alga, Mutimo cylindricus, was preserved even in high K+ seawater. This result indicates that none of the K+ channels is essential for male gamete chemotaxis in the brown alga, suggesting that the signalling mechanism for chemotaxis in this brown alga is quite different from that of marine invertebrates. Correlated to this result, we revealed that the channels previously proposed as homologues of tetraKCNG in brown algae have a distinct domain composition from that of the tetraKCNG. Namely, one of them possesses two repeats of the six transmembrane segments (diKCNG) instead of four. The structural analysis suggests that diKCNG is a cyclic nucleotide-modulated and/or voltage-gated K+ channel.