A Transient Receptor Potential Ion Channel in Chlamydomonas Shares Key Features with Sensory Transduction-Associated TRP Channels in Mammals

Abstract

Sensory modalities are essential for navigating through an ever-changing environment. From insects to mammals, transient receptor potential (TRP) channels are known mediators for cellular sensing. Chlamydomonas reinhardtii is a motile single-celled freshwater green alga that is guided by photosensory, mechanosensory, and chemosensory cues. In this type of alga, sensory input is first detected by membrane receptors located in the cell body and then transduced to the beating cilia by membrane depolarization. Although TRP channels seem to be absent in plants, C. reinhardtii possesses genomic sequences encoding TRP proteins. Here, we describe the cloning and characterization of a C. reinhardtii version of a TRP channel sharing key features present in mammalian TRP channels associated with sensory transduction. In silico sequence-structure analysis unveiled the modular design of TRP channels, and electrophysiological experiments conducted on Human Embryonic Kidney-293T cells expressing the Cr-TRP1 clone showed that many of the core functional features of metazoan TRP channels are present in Cr-TRP1, suggesting that basic TRP channel gating characteristics evolved early in the history of eukaryotes.

A TRP conductance modulates repolarization after sensory-dependent depolarization in Chlamydomonas reinhardtii

“…Both located at the cilia, Cr-TRPP2 participates in flagella-dependent mating behavior, 10 and Cr-TRP11 seems to be part of the mechanosensory response circuit. 11 Recently, Arias-Darraz and colleagues have cloned Cr-TRP1, 12 one of the most primitive versions of a TRP channel, demonstrating that the conservation of structural and functional features can be traced back early in eukaryote evolution. Given the importance of TRP channels in cellular sensing within the animal kingdom, we want to investigate their general role in the behavior of the algae.…”

“…This is in contrast to a previous study reporting 8 TRP channels, 11 and a recent study by our group reporting 10 TRP channels. 12 In the case of the latter, different assessment criteria with more stringent parameters were used to select for TRP channels. Reciprocal BLAST analysis of the 21 putative TRP channels indicates that Chlamydomonas contains TRP channels related to members of the TRPM and TRPV subfamilies: Chlamydomonas TRP5, TRP7, TRP11, TRP13, TRP16, TRP21, TRP22, TRP26, TRP27, and TRP28. In particular, our analysis suggests that TRP5 and TRP16 12 Phylogenetic reconstruction of the TRP channel family indicates that TRP1 belongs to an evolutionary distinct branch containing TRPC and TRPM channels.…”

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“…In protozoa, systematic analysis is scant and assignment to eukaryotic, specifically mammalian types is difficult. For the bikont Paramecium, originally no TRP channel genes had been found [106], but then three genes were retrieved [121]. Parasitic relatives of Paramecium, Apicomplexa, Toxoplasma gondii and probably also Plasmodium spp.…”

“…The green flagellate Chlamydomonas reinhardtii contains 19 genes encoding TRP channels [122], one of which shows considerable similarity to a human form and is localized probably in the flagellar membrane, contributing to sensory transduction [121]. Data mining revealed TRP channels encoding genes in Dictyostelium [121], where one of the members, PKD2, is localized in the cell surface and governs rheotaxis [123]. Choanoflagellates are endowed with TRP channels genes [124]; expanded molecular data mining revealed TRPA, TRPC, TRPM, TRPML and TRPV types [78].…”

“…Parasitic flagellates Leishmania and Trypanosoma also possess TRP channel, but for all unicellular parasites, molecular characterization is yet to be done [110]. The green flagellate Chlamydomonas reinhardtii contains 19 genes encoding TRP channels [122], one of which shows considerable similarity to a human form and is localized probably in the flagellar membrane, contributing to sensory transduction [121]. Data mining revealed TRP channels encoding genes in Dictyostelium [121], where one of the members, PKD2, is localized in the cell surface and governs rheotaxis [123].…”