Microbial arms race: Ballistic “nematocysts” in dinoflagellates represent a new extreme in organelle complexity by Gregory S. Gavelis, Kevin C. Wakeman,

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Microbial arms race: Ballistic “nematocysts” in dinoflagellates represent a new extreme in organelle complexity by Gregory S. Gavelis, Kevin C. Wakeman, Urban Tillmann, Christina Ripken, Satoshi Mitarai, Maria Herranz, Suat Özbek, Thomas Holstein, Patrick J. Keeling, and Brian S. Leander Science Volume 3(3):e1602552 March 31, 2017 Copyright © 2017, The Authors

Fig. 1 Diversity and independent origins of extrusomes. Diversity and independent origins of extrusomes. (A to E) Nematocysts in the dinoflagellate P. kofoidii, including a live whole cell (A) and a cell that was preserved in Lugol’s iodide solution while capturing a prey cell of A. tamarense (B). (C) Enhanced contrast image shows the defensive trichocysts deployed by A. tamarense (arrows) in response to attack by P. kofoidii. (D and E) Isolated nematocysts from P. kofoidii, seen as unfired (D) and discharged (E). (F to H) Nematocysts in the dinoflagellate Nematodinium sp., which have an eye-like ocelloid (F). A battery of nematocysts is visible in the live cell (G) and remains intact after cell lysis (H). (I) Genomic distribution of known extrusome proteins (vertical labels) across eukaryotes based on best reciprocal Basic Local Alignment Search Tool (BLAST) hits (black squares), which is a common predictor of protein homology. Taxa are listed within an established phylogenetic framework (38, 39). Gregory S. Gavelis et al. Sci Adv 2017;3:e1602552 Copyright © 2017, The Authors

Fig. 2 Reconstruction of the nematocysts in the dinoflagellate P Fig. 2 Reconstruction of the nematocysts in the dinoflagellate P. kofoidii. Reconstruction of the nematocysts in the dinoflagellate P. kofoidii. (A) SEM micrograph of a cell of P. kofoidii, including an armed taeniocyst (arrow) in the apical region that first contacts prey. (B) SEM micrograph of an isolated taeniocyst that has discharged its amorphous contents. (C) SEM micrograph of an isolated nematocyst that has become arrested very early in discharge; arrowhead, operculum. (D) FIB-SEM section of taeniocyst and nematocyst enclosed by a membranous chute (arrowhead) and (E) maximum intensity projection of the same region seen slightly from above and below (F). (G) Virtual dissection of the nematocyst-taeniocyst complex. Brackets indicate the membrane-bound compartments in which those components are grouped during early development. Later in development, compartments fuse to form the chute. Gregory S. Gavelis et al. Sci Adv 2017;3:e1602552 Copyright © 2017, The Authors

Fig. 3 Nematocyst discharge in Polykrikos. Nematocyst discharge in Polykrikos. (A) The putative ballistic sequence of nematocyst discharge is as follows: (1) striated capsule contracts; (2) internal pressure forces stylet to pierce capsule and open operculum (dark green); (3) part of the capsule everts; (4) stylet exits through the nozzle and detaches; and (5) mucilaginous tubule (blue) uncoils and is projected through the stylet base (yellow). Orange, relaxed capsule wall; red, contracted capsule wall. (B to E) SEM micrographs of isolated discharged nematocysts (B to D) and a nematocyst piercing a prey cell (E). Arrowhead, operculum; C, capsule; T, tubule. Gregory S. Gavelis et al. Sci Adv 2017;3:e1602552 Copyright © 2017, The Authors

Fig. 4 Reconstruction of the nematocysts in Nematodinium sp. Reconstruction of the nematocysts in Nematodinium sp. (A to E) Images derived from single-cell FIB-SEM. (A) Partial reconstruction of a cell with nematocysts shown in beige and mucocysts shown in purple. (B) Longitudinal FIB-SEM section through a cell showing the nucleus and nematocysts (arrowheads). (C) 3D maximum intensity projection showing a battery of nematocysts. (D) 3D tilted reconstruction of a nematocyst. (E) Longitudinal reconstruction of a nematocyst. (F to K) Single-cell TEM micrographs of a nematocyst in oblique section (F), cross section (G to J), and longitudinal section (K) showing the striated material (arrow) and variable symmetries across different nematocysts, with the number of subcapsules printed in the upper right corner. (L) A virtual dissection of the nematocyst components. Brackets indicate the membrane-bound compartments bounding the components indicated. (F) to (J) scale bar, 500 nm. Gregory S. Gavelis et al. Sci Adv 2017;3:e1602552 Copyright © 2017, The Authors