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A Subcellular Atlas of Toxoplasma Reveals the Functional Context of the Proteome

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A Subcellular Atlas of Toxoplasma Reveals the Functional Context of the Proteome bioRxiv preprint doi: https://doi.org/10.1101/2020.04.23.057125; this version posted April 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. A subcellular atlas of Toxoplasma reveals the functional context of the proteome Konstantin Barylyuk1*, Ludek Koreny1, Huiling Ke1, Simon Butterworth1, Oliver M. Crook1,2,3, Imen Lassadi1, Vipul Gupta1, Eelco Tromer1, Tobias Mourier4, Tim J. Stevens5, Lisa M. Breckels1,2, Arnab Pain4,6,7, Kathryn S. Lilley1,2, and Ross F. Waller1,8,* 1 Department of Biochemistry, University of Cambridge, United Kingdom 2 Milner Therapeutics Institute, Cambridge, United Kingdom 3 MRC Biostatistics Unit, Cambridge Institute for Public Health, Cambridge, United Kingdom 4 Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Saudi Arabia 5 MRC Laboratory of Molecular Biology, Cambridge, United Kingdom 6 Global Station for Zoonosis Control, GI-CoRE, Hokkaido University, Sapporo, Japan 7 Nuffield Division of Clinical Laboratory Sciences (NDCLS), University of Oxford, Headington, Oxford, United Kingdom 8 Lead author * Correspondence: [email protected], [email protected] ABSTRACT billion people at risk (World Health Organization, 2018). Cryptosporidiosis (Cryptosporidium spp.) is the second Apicomplexan parasites cause major human leading cause of fatal infant diarrhea affecting 800,000 disease and food insecurity. They owe their annually (Kotloff et al., 2013; Striepen, 2013). Toxoplasmosis (Toxoplasma gondii) occurs as chronic considerable success to novel, highly specialized infections in ~30% of the human population and can cause cell compartments and structures. These life-threatening congenital toxoplasmosis, fetal malform- adaptations drive their recognition and non- ation and abortion, blindness, and encephalitis (Havelaar et destructive penetration of host’s cells and the al., 2015). Furthermore, the economic damage of disease elaborate reengineering of these cells to promote in livestock caused by apicomplexans is estimated in growth, dissemination, and the countering of host billions of US dollars annually (Rashid et al., 2019). defenses. The evolution of unique apicomplexan Together these pathogens have a major effect on global cellular compartments is concomitant with vast health and prosperity, disproportionately affecting proteomic novelty that defines these new cell developing world regions. organizations and their functions. Consequently, Apicomplexans are deeply divergent organisms from half of apicomplexan proteins are unique and better-studied model eukaryotic cell systems and, as uncharacterized, and these cells are, therefore, very parasites and pathogens, have displayed superb ingenuity poorly understood. Here, we determine the steady- for generation and specialization of new cell structures and state subcellular location of thousands of proteins compartments. For example, a dedicated apical structure simultaneously within the globally prevalent enables non-destructive penetration and invasion of human apicomplexan parasite Toxoplasma gondii. This and animal cells. This ‘apical complex’ includes a battery of provides unprecedented comprehensive molecular different novel secretory compartments (micronemes, definition to these cells and their novel rhoptries, dense granules) for staged release of molecules compartments, and these data reveal the spatial required to search for, identify, penetrate and exploit the organizations of protein expression and function, host’s cells (Figure 1A) (Kats et al., 2008; Lebrun et al., adaptation to hosts, and the underlying evolutionary 2014). Apicomplexans have also developed novel gliding trajectories of these pathogens. motility structures anchored in a pellicular cytoskeleton (Frénal et al., 2017). Furthermore, modified versions of two canonical endosymbiotic compartments, the mitochondrion INTRODUCTION and a remnant of a photosynthetic plastid (apicoplast), have developed in response to the metabolic needs of obligate parasitism (Sheiner et al., 2013). Apicomplexa is a phylum of highly adapted unicellular eukaryotes specialized for intracellular parasitism in Apicomplexans have not only created novel organization animals (Votýpka et al., 2017). The remarkable success of and biochemistry of their own cell compartments. Via this group is evident by more than 6,000 described species secretion of complex mixtures of parasite proteins, they that infect potentially every vertebrate and most become active centers for subverting and remodeling the invertebrates (Votýpka et al., 2017). Many apicomplexans composition, organization, and properties of the host cells. cause devastating diseases in humans and livestock. Upon invasion of these host cells, they form, and typically Malaria, caused by Plasmodium spp., results in over remain within, a ‘parasitophorous vacuole’ decorated with 400,000 deaths and 200 million infections annually, with 3.2 secreted parasite proteins (Cesbron-Delauw et al., 2008). 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.23.057125; this version posted April 23, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Parasite-secreted proteins also target and modify existing Moreover, these data reveal the landscapes of cellular host cell compartments, including the nucleus, organization, function and evolution including gene mitochondrion, ER, cytoskeleton, and plasma membrane. expression programs, adaptative arms races with hosts, In doing so, they interfere with host control of defense and and the deeper evolutionary trajectories to parasitism, metabolism, cause reorganization of the host organelle providing a new level of insight into these parasites. positions and associations, change the mechanical properties of the host cell, and alter how infected cells interact with other human cells and tissues (Hakimi et al., RESULTS 2017; Pernas et al., 2014; Soni et al., 2016). This exquisite Whole-cell biochemical fractionation of Toxoplasma redefinition of host cells reflects 100s of millions of years of gondii extracellular tachyzoites co-evolution with their hosts and is orchestrated by the parasite secreted effector molecules delivered from the To determine if the steady-state subcellular locations of unique invasion machinery and compartments of these thousands of proteins could be simultaneously captured in parasites. Moreover, this adaptation is ongoing with apicomplexans, we adapted the hyperLOPIT method for contemporary changes and variability that confounds whole-cell spatial proteomics to Toxoplasma gondii adaptive immune responses and efforts to develop effective tachyzoites, the extracellular form of this parasite that is vaccines. primed for host cell invasion. The hyperLOPIT method exploits distinct abundance distribution profiles that The novelty and divergence of apicomplexan cell organelles and subcellular structures form upon compartments is concomitant with tremendous novelty of biochemical fractionation such as density-gradient genes and proteins. This severely limits inferences of the centrifugation. Proteins exhibiting similar distribution cell biology of these organisms that can be made from profiles of abundance through these fractions are assigned knowledge of better-studied model organisms. Indeed, to distinct subcellular structures (Christoforou et al., 2016; approximately half of apicomplexan proteins are known Mulvey et al., 2017). only as ‘hypotheticals’ and are unique to these cells (Swapna and Parkinson, 2017). Moreover, each apicom- To capture measurable variance of proteome profiles for plexan lineage possesses its own new proteins, the hyperLOPIT assignment, optimization of both cell disruption products of ongoing adaptation to specific hosts (Woo et al., methods and density gradient profiles were required. Using 2015). In such highly specialized cells, the subcellular several subcellular marker proteins, western blot analysis location and function of proteins are tightly linked. Yet, of cell homogenates separated by differential and density- despite decades of effort to understand the distribution of gradient centrifugation was used to determine suitable parasite proteins, typically relying on protein visualization conditions (Figure 1B). Apicomplexan infectious zoites by immunofluorescence microscopy (Woodcroft et al., such as Toxoplasma tachyzoites have a robust cell pellicle 2012), the complete proteomes of most parasite (Figure 1A) that is resistant to simple cell disruption by compartments remain very poorly known. Even the hypotonic lysis. Nitrogen cavitation (Lacombe et al., 2019; locations of proteins of predicted function based on Wang et al., 2014) was identified as the most effective, as conserved sequences in other organisms are largely well as non-heat-generating, method of cell disruption untested in apicomplexans. Thus, our understanding of the (Table S1). Membranous compartments and other cell biological complexity and functional organization of these particles were enriched from soluble cytosolic material by pathogens is severely limited by the lack of this basic discontinuous density centrifugation of the homogenate, information. and this particulate material was then fractionated on continuous linear density gradients of iodixanol resulting in The roles and importance of apicomplexans’ unique
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