Microtubule stabilizer reveals requirement of Ca2+-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae.

Mami Nomura,Kohei Atsuji,Kazuo Inaba,Ken-Ichiro Ishida,Takeshi Nakayama,Keiko Hirose,Kogiku Shiba,Ryuji Yanase

doi:10.1242/bio.036590

Abstract

ABSTRACTA haptonema is an elongated microtubule-based motile organelle uniquely present in haptophytes. The most notable and rapid movement of a haptonema is ‘coiling’, which occurs within a few milliseconds following mechanical stimulation in an unknown motor-independent mechanism. Here, we analyzed the coiling process in detail by high-speed filming and showed that haptonema coiling was initiated by left-handed twisting of the haptonema, followed by writhing to form a helix from the distal tip. On recovery from a mechanical stimulus, the helix slowly uncoiled from the proximal region. Electron microscopy showed that the seven microtubules in a haptonema were arranged mostly in parallel but that one of the microtubules often wound around the others in the extended state. A microtubule stabilizer, paclitaxel, inhibited coiling and induced right-handed twisting of the haptonema in the absence of Ca2+, suggesting changes in the mechanical properties of microtubules. Addition of Ca2+ resulted in the conversion of haptonematal twist into the planar bends near the proximal region. These results indicate that switching microtubule conformation, possibly with the aid of Ca2+-binding microtubule-associated proteins is responsible for rapid haptonematal coiling.

Highlights

Haptophytes are the group of microalgae that are widely distributed in oceans
We found that a microtubule stabilizer, paclitaxel, inhibits haptonematal coiling, suggesting that structural changes of the microtubules are responsible for the induction of rapid haptonema coiling
When compared with other Chrysochromulina species, such as National Institute for Environmental Studies (NIES)-1333, the haptonema of this species was more resistant to mechanical stimuli that cause detachment from the cell body

Summary

Introduction

Haptophytes are the group of microalgae that are widely distributed in oceans. They show similarities to heterokonts in chloroplast structure and chlorophyll species but are classified into an independent phylum owing to several cytological properties, including the lack of mastigonemes on flagella and the presence of extracellular scales or coccoliths (Christensen, 1962; Andersen, 2004). A haptonema is a filiform organelle uniquely present in haptophytes (Parke et al, 1955). When haptophytes receive mechanical stimuli, they fully coil the haptonema within only a few milliseconds. The coiled state is thought to be a low-energy form, because the haptonema is always coiled when it is detached or when haptophytes are dead (Estep and MacIntyre, 1989)

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Results

Conclusion