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Ubiquitous distribution of helmchrome in phototactic swarmers of the stramenopiles

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Abstract

Most swarmers (swimming cells) of the stramenopile group, ranging from unicellular protist to giant kelps (brown algae), have two heterogeneous flagella: a long anterior flagellum (AF) and a relatively shorter posterior flagellum (PF). These flagellated cells often exhibit phototaxis upon light stimulation, although the mechanism by which how the phototactic response is regulated remains largely unknown. A flavoprotein concentrating at the paraflagellar body (PFB) on the basal part of the PF, which can emit green autofluorescence under blue light irradiance, has been proposed as a possible blue light photoreceptor for brown algal phototaxis although the nature of the flavoprotein still remains elusive. Recently, we identified helmchrome as a PF-specific flavoprotein protein in a LC-MS/MS-based proteomics study of brown algal flagella (Fu et al. 2014). To verify the conservation of helmchrome, in the present study, the absence or presence and the localization of helmchrome in swarmers of various algal species were investigated. The results showed that helmchrome was only detected in phototactic swarmers but not the non-phototactic ones of the stramenopile group. Electron microscopy further revealed that the helmchrome detectable swarmers bear a conserved PFB-eyespot complex, which may serve as structural basis for light sensing. It is speculated that all three conserved properties: helmchrome, the PFB structure, and the eyespot apparatus, will be essential parts for phototaxis of stramenopile swarmers.

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Abbreviations

AUREO:

Aureochrome

bZIP:

Basic leucine zipper

ChR:

Channelrhodopsin

DAPI:

4′,6-Diamidino-2-phenylindole

HELMC:

Helmchrome

LOV:

Light-oxygen-voltage sensing

PAC:

Photoactivated adenylyl cyclase

PAS:

Per-ARNT-Sim

PFB:

Paraflagellar body

PHOT:

Phototropin

PHY:

Phytochrome

RGS:

Regulator of G protein signaling

VVD:

Vivid

WC:

White collar

ZnF:

Zinc finger

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Acknowledgments

We would like to thank Dr. Hidetoshi Okuyama, Faculty of Environmental Earth Science, Hokkaido University, for kindly providing the Thraustochytrid-like 12B strain. We also thank Dr. J. Mark Cock, University Pierre et Marie Curie and Centre National de la Recherche Scientifique, France, who kindly gave us many valuable comments and corrected our English.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran, 051-0013, Japan

    Gang Fu, Chikako Nagasato & Taizo Motomura

  2. Research Center for Inland Seas, Kobe University, Rokkodai, Nadaku, Kobe, 657-8501, Japan

    Takahiro Yamagishi & Hiroshi Kawai

  3. Graduate School of Integrated Arts and Sciences, Kochi University, Kochi, 780-8520, Japan

    Kazuo Okuda

  4. Faculty of Marine Bioscience, Fukui Prefectural University, Obama, 917-0003, Japan

    Yoshitake Takao

  5. Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Takeo Horiguchi

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  1. Gang Fu
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Correspondence to Taizo Motomura.

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Supplementary Fig. S1

Immunofluorescence microscopy images of 25 swarmers investigated. Images of α-tubulin (red), helmchrome (green), and merged with DAPI (blue) are shown for each sample. The cells are orientated with the AF extending upwards and the PF extending opposite. a Female gamete of Scytosiphon lomentaria. b Female gamete of Culteria cylindrica. c Zoospores of Desmarestia ligulata. d Sperm of Silvetia babingtonii. e Zoospore of Chorda filum. f Zoospore of Saccharina angustata. g Zoospore of Undaria pinnatifida. h Zoospore of Alaria crassifolia. i Zoospore of Agarum clathratum. j Dinobryon sertularia. k Dinobryon sociale. l Zoospore of Thraustochytrid-like 12B. m Zoospore of Sicyoidochytrium sp. n Zoospore of Ulkenia amoeboidea. o Zoospore of Parietichytrium sp. p HG193 Symbiodinium sp. q HG243 Symbiodinium sp. r HG241 Bysmatrum sp. s TM106 Gymnodinium sp. t Male gamete of Ulva pertusa. u Female gamete of Ulva pertusa. v Female gamete of Bryopsis plumosa. w Chrysochromulina hirta. Scale bars, 5 μm. (GIF 266 kb).

High resolution image (EPS 31304 kb).

Supplementary Fig. S2

Electron microscopy image of a Ulva pertusa gamete. Note the association of eyespot and flagella is different from that of phototactic brown algal swarmers. Ch, chloroplast; Es, eyespot; F, flagellum; M, mitochondria. Scale bar, 500 nm. (GIF 95 kb).

High resolution image (EPS 7075 kb).

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Fu, G., Nagasato, C., Yamagishi, T. et al. Ubiquitous distribution of helmchrome in phototactic swarmers of the stramenopiles. Protoplasma 253, 929–941 (2016). https://doi.org/10.1007/s00709-015-0857-7

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