Predatory Protists the Two Words Used in the Main Title Grell, K.G
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Current Biology Magazine Chalker, D.L., and Yao, M.C. (2011). DNA Modes of feeding in predatory elimination in ciliates: transposon Primer domestication and genome surveillance. Annu. protists Rev. Genet. 45, 227–246. Predatory protists The two words used in the main title Grell, K.G. (1979). Cytogenetic systems and have defi nitions of convenience. Use evolution in foraminifera. J. Foram. Res. 9, 1–13. of the term ‘protist’ here refers to Hamilton, E.P., Kapusta, A., Huvos, P.E., Brian S. Leander all (mostly single-celled) eukaryotes Bidwell, S.L., Zafar, N., Tang, H., Hadjithomas, M., Krishnakumar, V., excluding the following multicellular Badger, J.H., Caler, E.V., et al. (2016). Among the most impactful events in lineages: green algae/land plants, Structure of the germline genome of the history of life was the evolutionary animals, fungi, brown algae and red Tetrahymena thermophila and relationship to the massively rearranged somatic genome. origin of phagotrophy over a billion algae. Use of the term ‘predator’ eLife 5, e19090. years ago, which triggered the ability refers to eukaryotes capable of Iwamoto, M., Hiraoka, Y., and Haraguchi, T. (2016). of a cell to ingest a particle of organic hunting and ingesting relatively Uniquely designed nuclear structures of lower eukaryotes. Curr. Opin. Cell Biol. 40, 66–73. material, whether dead or alive, as large prey cells. Different kinds of Iwamoto, M., Koujin, T., Osakada, H., Mori, C., food. Without it, there would be no predators represent vastly distantly Kojidani, T., Matsuda, A., Asakawa, H., Hiraoka, Y., and Haraguchi, T. (2015). Biased animals and no plants, let alone the related lineages across the tree of assembly of the nuclear pore complex is vast number of single-celled lineages of eukaryotes, and this general lifestyle required for somatic and germline nuclear eukaryotes that either photosynthesize can blend into the defi nitions of other differentiation in Tetrahymena. J. Cell Sci. 128, 1812–1823. and/or consume other organisms to modes of nutrition, such as stalked Keeling, P.J., and Burki, F. (2019). Progress sustain themselves long enough to suspension feeding and parasitism. towards the tree of eukaryotes. Curr. Biol. 29, reproduce. In fact, the most recent Although parasites are smaller than R808–R817. Klobutcher, L.A., and Herrick, G. (1997). common ancestor of all eukaryotes and usually do not kill their hosts, Developmental genome reorganization in was almost certainly capable of some predators and parasites use the ciliated protozoa: the transposon link. Prog. Nucleic Acid Res. Mol. Biol. 56, 1–62. phagotrophy, a trait that fundamentally same feeding mechanism to extract Maurer-Alcala, X.X., Yan, Y., Pilling, O.A., distinguishes eukaryotes from all other nutrients from prey cells and host Knight, R., and Katz, L.A. (2018). Twisted tales: forms of life, namely archaea and cells, respectively, which can blur the insights into genome diversity of ciliates using single-cell ‘omics. Genome Biol. Evol. 10, bacteria. distinction between the two lifestyles. 1927–1939. The evolution of phagotrophy was For instance, the ability to feed like Maurer-Alcala, X.X., and Nowacki, M. (2019). Evolutionary origins and impacts of genome predicated by a dynamic proteinaceous a vampire by piercing the surface of architecture in ciliates. Ann. NY Acad. Sci. cytoskeleton comprising microtubules, a cell and sucking out its contents 1447, 110–118. actin fi laments and associated as food, known as ‘myzocytosis’, Prescott, D.M. (1994). The DNA of ciliated protozoa. Microbiol. Rev. 58, 233–267. molecular motors, which together is found in several different kinds of Raikov, I.B. (1985). Primitive never-dividing preceded the origin of other distinctive predators, such as didinid ciliates, macronuclei of some lower ciliates. Int. Rev. traits of eukaryotes, such as the colpodellids, colponemids, noctilucoid Cytol. 95, 267–325. Singh, D.P., Saudemont, B., Guglielmi, G., nucleus, endomembrane system dinofl agellates and vampyrellid Arnaiz, O., Goût, J.F., Prajer, M., Potekhin, A., and mitochondria. Phagotrophy also cercozoans, and some marine intestinal Przybòs, E., Aubusson-Fleury, A., Bhullar, S., et al. (2014). Genome-defence small facilitated major evolutionary events parasites, such as archigregarine RNAs exapted for epigenetic mating type that transformed the diversity of life and apicomplexans. inheritance. Nature 509, 447–452. the planet as a whole, such as multiple A modifi cation of myzocytosis Vogt, A., Goldman, A.D., Mochizuki, K., and Landweber, L.F. (2013). Transposon origins of photosynthesis and multiple involves a free-living predator, such domestication versus mutualism in ciliate independent origins of parasitism as some colpodellids, perforating and genome rearrangements. PLoS Genet. 9, across the tree of eukaryotes. entering a prey cell and eating it from e1003659. Warren, A., Patterson, D.J., Dunthorn, M., However, despite these major the inside out, leaving only an empty Clamp, J.C., Achilles-Day, U.E.M., Aescht, E., events, many different lineages of shell of what once was. This particular Al-Farraj, S.A., Al-Quraishy, S., Al-Rasheid, K., Carr, M., et al. (2017). Beyond the “code”: a eukaryotes have maintained lifestyles feeding strategy is also found in the guide to the description and documentation most consistent with their deepest zoospores of some parasites, such of biodiversity in ciliated protists (Alveolata, ancestors in the form of free-living as perkinsozoan alveolates; after Ciliophora). J. Eukaryot. Microbiol. 64, 539–554. predators capable of hunting, killing and entering the host cell, the zoospores Xiong, J., Yang, W., Chen, K., Jiang, C., Ma, Y., consuming other prey organisms. This feed on the cell contents and grow Chai, X., Yan, G., Wang, G., Yuan, D., Liu, Y., et al. (2019). Hidden genomic evolution in general mode of nutrition in single-celled a large multicellular sporangium that a morphospecies-The landscape of rapidly eukaryotes has resulted in dynamic completely fi lls the inside of the now evolving genes in Tetrahymena. PLoS Biol. 17, predator–prey relationships and a exterminated host cell. New zoospores e3000294. diverse array of traits associated with are then released from the mature their feeding apparatus, motility systems sporangium and hunt for a new host 1Department of Molecular Genetics and Cell and hunting mechanisms. A brief cell to perpetuate the parasitic lifecycle. Biology, University of Chicago, Chicago, survey of these traits across the tree of Evidence of myzocytosis in the form IL 60637, USA. 2Department of Molecular, eukaryotes is the focus of this primer in of perforations in the protective shells Cellular and Developmental Biology, order to introduce the reader to some of other protists shows up in the fossil University of California Santa Barbara, outstanding examples of convergent record about 750 million years ago. Santa Barbara, CA 93106, USA. 3Institute of Molecular Biology, Academia Sinica, Taipei, evolution, structural complexity and Many different lineages of predatory Taiwan. behavioral sophistication within the protists acquire food using whole *E-mail: [email protected] microbial world. prey cell phagocytosis, which is R510 Current Biology 30, R451–R520, May 18, 2020 Crown Copyright © 2020 Published by Elsevier Inc. Current Biology Magazine Figure 1. Montage of some predatory protists of bacteria and their traits. (A) Light micrograph of the bicosoecid Cantina showing two fl agella (double arrowheads) and the ventral groove (arrow) used to feed on bacteria (image courtesy of Yubuki and Leander). (B) Scanning electron micrograph of the excavate Aduncisulcus in ventral view showing the ventral groove and two fl agella (double arrowhead) (image courtesy of Yubuki and Leander). (C,D) Scanning electron micrographs of the excavate Kipferlia showing a rod-shaped bacterium (arrowhead) trapped in the ventral groove (C) and drawn into the mouth-like cell opening (D) (image courtesy of Yubuki and Leander). Scale bars: A = 8 µm, B = 2 µm, C,D = 1 µm. accomplished in a diverse number of As predatory protists evolved more In addition to armor, many prey cells ways. Predators capable of eating large sophisticated feeding strategies, their defend themselves with subcellular prey cells, such as other eukaryotes, preferred eukaryotic prey evolved more weapons, called ‘extrusive organelles’, tend to have specialized structures sophisticated forms of evasion and that come in many different forms, to facilitate this feat. For instance, protection. Multicellular aggregations, such as the coiled ejectisomes of crawling amoebae ooze dynamic for instance, in the form of fi laments, cryptomonads and the telescopic pseudopods around prey cells in prostrate sheets and arborescent trichocysts of alveolates. The rapid their path. Some dinofl agellates unzip arrays create larger body sizes that discharge of extrusive organelles specifi c regions of their otherwise rigid limit the abilities of protistan predators from prey cells serves to both repel cells to internalize prey cells. Some to feed on them; as such, protistan a predatory attack like a shield dinofl agellates (e.g., Protoperidinium, predators were likely a major selective and forcefully propel the prey cell Gyrodinium) use a large hood-like cell driver for the independent origins in unpredictable directions and extension, called a ‘pallium’, to envelop of multicellularity across the tree of away from the pursuing predator. fi lamentous prey and enzymatically fold eukaryotes. Larger