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Sci Adv. 2017 Mar 31;3(3):e1602552. doi: 10.1126/sciadv.1602552. eCollection 2017 Mar.

Microbial arms race: Ballistic "nematocysts" in dinoflagellates represent a new extreme in organelle complexity.

Author information

1
Department of Botany, University of British Columbia, Vancouver, Canada.
2
Department of Zoology, University of British Columbia, Vancouver, Canada.
3
Office of International Affairs, Hokkaido University, Kita 10, Nishi 8, Sapporo 060-0810, Japan.
4
Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany.
5
Faculty of Science, Hokkaido University, Kita 10, Nishi 8, Sapporo 060-0810, Japan.
6
Marine Biophysics Unit, Okinawa Institute of Science and Technology, Okinawa, Japan.
7
Centre for Organismal Studies, University of Heidelberg, Heidelberg, Germany.

Abstract

We examine the origin of harpoon-like secretory organelles (nematocysts) in dinoflagellate protists. These ballistic organelles have been hypothesized to be homologous to similarly complex structures in animals (cnidarians); but we show, using structural, functional, and phylogenomic data, that nematocysts evolved independently in both lineages. We also recorded the first high-resolution videos of nematocyst discharge in dinoflagellates. Unexpectedly, our data suggest that different types of dinoflagellate nematocysts use two fundamentally different types of ballistic mechanisms: one type relies on a single pressurized capsule for propulsion, whereas the other type launches 11 to 15 projectiles from an arrangement similar to a Gatling gun. Despite their radical structural differences, these nematocysts share a single origin within dinoflagellates and both potentially use a contraction-based mechanism to generate ballistic force. The diversity of traits in dinoflagellate nematocysts demonstrates a stepwise route by which simple secretory structures diversified to yield elaborate subcellular weaponry.

KEYWORDS:

Convergent evolution; cnidocyst; extrusome; minicollagen; mucocyst; red queen; secretion; secretory; trichocyst

PMID:
28435864
PMCID:
PMC5375639
DOI:
10.1126/sciadv.1602552
[Indexed for MEDLINE]
Free PMC Article

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