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A Mutagenesis Screen for Essential Plastid Biogenesis Genes in Human Malaria Parasites

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A Mutagenesis Screen for Essential Plastid Biogenesis Genes in Human Malaria Parasites A mutagenesis screen for essential plastid biogenesis genes in human malaria parasites The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation Tang, Yong et al. "A mutagenesis screen for essential plastid biogenesis genes in human malaria parasites." PloS one 17 (2019): journal.pbio.3000136 © 2019 The Author(s) As Published 10.1371/journal.pbio.3000136 Publisher Public Library of Science (PLoS) Version Final published version Citable link https://hdl.handle.net/1721.1/124521 Terms of Use Creative Commons Attribution 4.0 International license Detailed Terms https://creativecommons.org/licenses/by/4.0/ METHODS AND RESOURCES A mutagenesis screen for essential plastid biogenesis genes in human malaria parasites 1 2 1 1 Yong TangID , Thomas R. MeisterID , Marta WalczakID , Michael J. Pulkoski-Gross , 3 3 4 1,4,5,6 Sanjay B. HariID , Robert T. Sauer , Katherine Amberg-JohnsonID , Ellen Yeh * 1 Department of Biochemistry, Stanford University School of Medicine, Stanford, California, United States of America, 2 Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California, United States of America, 3 Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America, 4 Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, United States of America, a1111111111 5 Department of Pathology, Stanford University School of Medicine, Stanford, California, United States of a1111111111 America, 6 Chan Zuckerberg Biohub, San Francisco, California, United States of America a1111111111 a1111111111 * [email protected] a1111111111 Abstract Endosymbiosis has driven major molecular and cellular innovations. Plasmodium spp. para- OPEN ACCESS sites that cause malaria contain an essential, non-photosynthetic plastidÐthe apicoplastÐ Citation: Tang Y, Meister TR, Walczak M, Pulkoski- which originated from a secondary (eukaryote±eukaryote) endosymbiosis. To discover Gross MJ, Hari SB, Sauer RT, et al. (2019) A organellar pathways with evolutionary and biomedical significance, we performed a muta- mutagenesis screen for essential plastid biogenesis genesis screen for essential genes required for apicoplast biogenesis in Plasmodium falcip- genes in human malaria parasites. PLoS Biol 17(2): e3000136. https://doi.org/10.1371/journal. arum. Apicoplast(−) mutants were isolated using a chemical rescue that permits conditional pbio.3000136 disruption of the apicoplast and a new fluorescent reporter for organelle loss. Five candidate Academic Editor: Boris Striepen, University of genes were validated (out of 12 identified), including a triosephosphate isomerase (TIM)- Georgia, UNITED STATES barrel protein that likely derived from a core metabolic enzyme but evolved a new activity. Published: February 6, 2019 Our results demonstrate, to our knowledge, the first forward genetic screen to assign essen- tial cellular functions to unannotated P. falciparum genes. A putative TIM-barrel enzyme and Copyright: © 2019 Tang et al. This is an open access article distributed under the terms of the other newly identified apicoplast biogenesis proteins open opportunities to discover new Creative Commons Attribution License, which mechanisms of organelle biogenesis, molecular evolution underlying eukaryotic diversity, permits unrestricted use, distribution, and and drug targets against multiple parasitic diseases. reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Raw sequencing data are available via the SRA repository (accession number PRJNA513880). Raw FACS files and Author summary gating schemes in main figures are available via the parasites, which cause malaria, and related apicomplexan parasites evolved FLowRepository (repository ID FR-FCM-ZYUH). Plasmodium Code for whole-genome sequencing analysis is from photosynthetic algae that acquired their chloroplast through two successive endo- available at https://github.com/yehlabstanford/ symbioses. Although no longer photosynthetic, the apicomplexan plastidÐor apicoplast biogenesis_screen. All other relevant data are Ðwas retained in these pathogens and provides critical metabolites during host cell infec- within the paper and its Supporting Information tion. The apicoplast is of major interest for its unique biology and potential to yield new files. antimalarial drug targets. Here, we focused on the critical genes required to grow, divide, Funding: This project has been funded with federal and inherit new apicoplasts during parasite replication. Given the apicoplast's divergent funds from the National Institute of Allergy and evolution, most of these cannot be recognized by their homology to genes with known Infectious Diseases (NIAID), National Institute of functions. Instead, we overcame significant technical challenges in the Plasmodium General Medical Sciences (NIGMS), and Director's PLOS Biology | https://doi.org/10.1371/journal.pbio.3000136 February 6, 2019 1 / 27 Plastid biogenesis genes in malaria parasites Fund, National Institutes of Health, Department of Health and Human Services under Award Numbers experimental system to perform an unbiased screen to search for these critical genes. Our 1K08AI097239 (EY), 1DP5OD012119 (EY), screen has uncovered new genes with intriguing evolution and function that open up AI016892 (RTS), F32GM116241 (SBH), opportunities to understand and ultimately exploit apicoplast biology. Finally, assigning T32GM007276 (KAJ and TRM), GM007365 (YT), and S10OD018220 (Stanford Functional Genomics new, essential gene functions in Plasmodium parasites remains a daunting task. The suc- Facility). Funding was also provided by the cessful identification of essential gene functions using an unbiased approach in this study Burroughs-Wellcome Fund (EY), Chan Zuckerberg provides a viable route for expansion of this screen or developing screens for other novel Biohub (EY), and the Stanford Bio-X SIGF William Plasmodium pathways in the future. and Lynda Steere Fellowship (KAJ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Introduction Competing interests: The authors have declared Plasmodium spp., which cause malaria, and related apicomplexan parasites are important that no competing interests exist. human and veterinary pathogens. These disease-causing protozoa are highly divergent from well-studied model organisms that are the textbook examples of eukaryotic biology, such that Abbreviations: ACP, acyl-carrier protein; ACPL, ACP leader peptide; amr, apicoplast-minus IPP- parasite biology often reveals striking eukaryotic innovations. The apicoplast, a nonphotosyn- rescued; AS, anthranilate synthase; ATc, thetic plastid found in apicomplexa, is one such ªinventionº [1, 2]. These intracellular parasites anhydrotetracycline; Atg8, autophagy-related evolved from photosynthetic algae that acquired their plastids through secondary endosymbio- protein 8; CcssrA, C. caldarium ssrA peptide; Clp, sis [3]. During secondary endosymbiosis, a chloroplast-containing alga, itself the product of caseinolytic protease; ClpC, Clp chaperone; ClpP, primary endosymbiosis, was taken up by another eukaryote to form a secondary plastid [4]. Clp protease; CRISPRi, Clustered Regularly Despite the loss of photosynthesis in apicomplexans, the apicoplast contains several prokary- Interspaced Palindromic Repeats interference; DMSO, dimethyl sulfoxide; EMS, ethyl otic metabolic pathways, is essential for parasite replication during human infection, and is a methanesulfonate; DOZI, development of zygote target of antiparasitic drugs [5±8]. inhibited; EcssrA, E. coli ssrA peptide; ENU, N- There are many traces of the apicoplast's quirky evolution in its present-day cell biology, in ethyl-N-nitrosourea; ER, endoplasmic reticulum; particular the pathways for its biogenesis. Like other endosymbiotic organelles, the single api- ERAD, ER-associated degradation; FACS, coplast cannot be formed de novo and must be inherited by its growth, division, and segrega- fluorescence-activated cell sorting; GST, glutathione S-transferase; HA, hemagglutinin; tion into daughter cells. The few molecular details we have about apicoplast biogenesis hint at IGPS, indole-3-glycerol phosphate synthase; IPTG, the major innovations that have occurred in the process of adopting and retaining this second- isopropyl β-D-1-thiogalactopyranoside; IPP, ary plastid. The apicoplast is bound by four membranes acquired through successive endosym- isopentenyl diphosphate; MCM, minichromosome bioses, such that apicoplast proteins transit through the endoplasmic reticulum (ER) and use a maintenance; ND, not determined; NGS, next symbiont-derived ER-associated degradation (ERAD)-like machinery (SELMA) to cross the generation sequencing; PD, protein degradation; two new outer membranes [9]. Curiously, autophagy-related protein 8 (Atg8), a highly con- PfFtsH1, P. falciparum ATP-dependent zinc metalloprotease 1; PRT, served eukaryotic protein and key marker of autophagosomes, localizes to the apicoplast and is phosphoribosyltransferase; RAP, RNA-binding required for its inheritance in Plasmodium and the related apicomplexan parasite Toxoplasma domain abundant in Apicomplexans; RBC, red gondii [10±12]. While SELMA and PfAtg8 are clear examples of molecular evolution in action, blood cell; RNAi, RNA interference; SELMA, other
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