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

Published online by Cambridge University Press:  18 July 2019

Nana Kinoshita-Terauchi ,
Kogiku Shiba ,
Makoto Terauchi ,
Francisco Romero ,
Héctor Vincente Ramírez-Gómez ,
Manabu Yoshida ,
Taizo Motomura ,
Hiroshi Kawai  and
Takuya Nishigaki Open the ORCID record for Takuya Nishigaki [Opens in a new window]
Nana Kinoshita-Terauchi
Affiliation:
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda City, Shizuoka 415-0025, Japan
Kogiku Shiba
Affiliation:
Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda City, Shizuoka 415-0025, Japan Misaki Marine Biological Station, Graduate School of Science, University of Tokyo, Miura, Kanagawa 238-0225, Japan
Makoto Terauchi
Affiliation:
Kobe University Research Center for Inland Seas, Rokkodai, Kobe 657-8501, Japan Center for Genome Informatics, Joint Support-Center for Data Science Research, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540, Japan
Francisco Romero
Affiliation:
Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico
Héctor Vincente Ramírez-Gómez
Affiliation:
Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico
Manabu Yoshida
Affiliation:
Misaki Marine Biological Station, Graduate School of Science, University of Tokyo, Miura, Kanagawa 238-0225, Japan
Taizo Motomura
Affiliation:
Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran 051-0013, Hokkaido, Japan
Hiroshi Kawai
Affiliation:
Kobe University Research Center for Inland Seas, Rokkodai, Kobe 657-8501, Japan
Takuya Nishigaki*
Affiliation:
Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico
*
*Address for correspondence: Takuya Nishigaki. Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico. Tel: +52 777 3291709. E-mail: [email protected]
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Summary

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.

Keywords

ChemotaxisCNGK channelHyperpolarizationMembrane potentialTetraKCNG channel
Type
Research Article
Information
Zygote , Volume 27 , Issue 4 , August 2019 , pp. 225 - 231
Copyright
© Cambridge University Press 2019 

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