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Quantitative Proteomic Map of the Trypanosomatid Strigomonas Culicis

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Quantitative Proteomic Map of the Trypanosomatid Strigomonas Culicis Protist, Vol. 170, 125698, December 2019 http://www.elsevier.de/protis Published online date 1 November 2019 ORIGINAL PAPER Quantitative Proteomic Map of the Trypanosomatid Strigomonas culicis: The Biological Contribution of its Endosymbiotic Bacterium a,2 b,2 a,c,d,2 Giselle V.F. Brunoro , Rubem F.S. Menna-Barreto , Aline S. Garcia-Gomes , d e,3 e a Carolina Boucinha , Diogo B. Lima , Paulo C. Carvalho , André Teixeira-Ferreira , a a f g Monique R.O. Trugilho , Jonas Perales , Veit Schwämmle , Marcos Catanho , h i d,1,4 Ana Tereza R. de Vasconcelos , Maria Cristina M. Motta , Claudia M. d’Avila-Levy , and a,1 Richard H. Valente a Laboratory of Toxinology, IOC, Oswaldo Cruz Foundation (FIOCRUZ), Rio de Janeiro, RJ 21040-900, Brazil b Laboratory of Cellular Biology, IOC, Oswaldo Cruz Foundation (FIOCRUZ), Rio de Janeiro, RJ 21040-900, Brazil c Laboratório de Microbiologia, Instituto Federal de Educac¸ão, Ciência e Tecnologia do Rio de Janeiro (IFRJ), Departamento de Alimentos, Rio de Janeiro, RJ 20270-021, Brazil d Laboratory of Integrated Studies in Protozoology, IOC, Oswaldo Cruz Foundation (FIOCRUZ), Rio de Janeiro, RJ 21040-900, Brazil e Laboratory for Structural and Computational Proteomics, ICC, Oswaldo Cruz Foundation (FIOCRUZ), Paraná, PR 81350-010, Brazil f Department for Biochemistry and Molecular Biology, University of Southern Denmark, Odense 5230, Denmark g Laboratory of Molecular Genetics of Microrganisms, IOC, Oswaldo Cruz Foundation (FIOCRUZ), Rio de Janeiro, RJ 21040-900, Brazil h National Laboratory for Scientific Computing, Petrópolis, RJ 25651-075, Brazil i Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, RJ 21491-590, Brazil Submitted May 17, 2019; Accepted October 20, 2019 Monitoring Editor: Dmitri Maslov 1 Corresponding authors; 2 These authors contributed equally to this work. 3 Present address: Mass Spectrometry for Biology Unit, CNRS, USR 2000, Institut Pasteur, Paris 75015, France 4 Present temporary address: de Duve Institute, Université Catholique de Louvain, Brussels 1200, Belgium e-mails [email protected] (C.M. d’Avila-Levy), [email protected] (R.H. Valente). Abbreviations: SC, Strigomonas culicis; CKB, Candidatus Kinetoplastibacterium blastocrithidii; CKC, Candidatus Kinetoplastibacterium crithidii; WT, Wild type; Apo, Aposymbiotic; lag phase, Well-defined adaptation phase; log phase, Exponential phase; GO, Gene Ontology; ETS, Electron transport system; ROS, Reactive oxygen species; LIT, Liver infusion and tryptose medium; PSM, Peptide-spectrum matching. https://doi.org/10.1016/j.protis.2019.125698 1434-4610/© 2019 Elsevier GmbH. All rights reserved. 2 G.V.F. Brunoro et al. Strigomonas culicis is a kinetoplastid parasite of insects that maintains a mutualistic association with an intracellular symbiotic bacterium, which is highly integrated into the protist metabolism: it furnishes essential compounds and divides in synchrony with the eukaryotic nucleus. The protist, conversely, can be cured of the endosymbiont, producing an aposymbiotic cell line, which presents a diminished ability to colonize the insect host. This obligatory association can represent an intermedi- ate step of the evolution towards the formation of an organelle, therefore representing an interesting model to understand the symbiogenesis theory. Here, we used shotgun proteomics to compare the S. culicis endosymbiont-containing and aposymbiotic strains, revealing a total of 11,305 peptides, and up to 2,213 proteins (2,029 and 1,452 for wild type and aposymbiotic, respectively). Gene ontology associated to comparative analysis between both strains revealed that the biological processes most affected by the elimination of the symbiont were the amino acid synthesis, as well as protein synthesis and folding. This large-scale comparison of the protein expression in S. culicis marks a step forward in the comprehension of the role of endosymbiotic bacteria in monoxenous trypanosomatid biology, particularly because trypanosomatids expression is mostly post-transcriptionally regulated. Key words: Strigomonas culicis; endosymbiont-bearing trypanosomatid; proteomics; amino acid and protein syntheses; protein folding; energy metabolism. © 2019 Elsevier GmbH. All rights reserved. Introduction tids, organelles that have a symbiogenetic origin (López-García et al. 2017; Margulis and Bermudes The Trypanosomatidae family (Kinetoplastea: Tr y- 1985). The endosymbiosis in trypanosomatids is panosomatida) comprises parasites of vertebrates, a mutualistic association and this intricate inter- invertebrates or plants. From the more than 20 for- action possesses several characteristics which mally described genera, two display species that probably configure an intermediate step of the are the causative agents of Chagas disease (Tr y- evolution towards the formation of an organelle panosoma cruzi), several types of leishmaniases (de Souza and Motta 1999; Harmer et al. 2018; (Leishmania spp.), and Human African Trypanoso- Motta 2010; Motta et al. 2013; Yurchenko and miasis (Trypanosoma brucei sensu lato). These Lukesˇ 2018). Therefore, it is not surprising that parasites alternate their life cycles between an the first description of an endosymbiont, as diplo- insect vector and a mammalian host, affecting ca. somes in Strigomonas culicis (Novy et al. 1907), 22 million people worldwide (Rodrigues et al. 2014). propelled the research in endosymbiont-harboring Nonetheless, the largest biodiversity of this protist trypanosomatids. family is among trypanosomatids that usually carry Another fact that also furthered symbiosis out their entire life cycle in insects (D’Avila-Levy research in trypanosomatids is the possibility of et al. 2015; Maslov et al. 2019). bacteria removal by antibiotic treatment, which Among insect trypanosomatids, members of the allows the obtainment of aposymbiotic strains that Strigomonadinae subfamily form a monophyletic can be maintained only in vitro. Such cured cells clade composed of the genera Angomonas, can be used as comparative models to understand Strigomonas, and Kentomonas, which have how the symbiont influences the host trypanoso- in common the presence of an endosymbiotic matid structure and physiology (Bombac¸a et al. ␤ -proteobacterium, Candidatus Kinetoplastibac- 2017; Chang and Trager 1974; D’Avila-Levy et al. terium spp. (Maslov et al. 2013; Teixeira et al. 2011; 2005a, b; Loyola-Machado et al. 2017; Motta 2010; Votypka´ et al. 2014). Recently, a new kinetoplastid- Yurchenko and Lukesˇ 2018). Up to now, all attempts bacterium association has been reported for to cultivate the bacteria alone have demonstrated another trypanosomatid species (Novymonas that these endosymbionts have a strict dependence esmeraldas); however, it is evolutionarily and on the protist host, being unable to survive out- phylogenetically divergent, when compared to side the trypanosomatids (reviewed in Motta 2010). the members of the Strigomonadinae subfamily, Trypanosomatids from the subfamily Strigomonad- and probably configures a completely different inae bear only a single bacterium in the cytoplasm, biological interaction (Kostygov et al. 2016, 2017). which is vertically transmitted after a synchronous Bacterial endosymbionts play a critical role in division with the host cell. The intracellular localiza- eukaryote evolution, which is illustrated by the tion of the bacterium is not random, being closely widespread occurrence of mitochondria and plas- associated to the cellular nucleus and surrounded Strigomonas culicis Differential Proteome 3 by glycosomes (Brum et al. 2014; Catta-Preta matids have provided a significant improvement in et al. 2015; Loyola-Machado et al. 2017; Motta the understanding of this mutualistic association et al. 2010). The presence of the endosymbiont (Motta et al. 2013; Penha et al. 2016). Addition- in trypanosomatids is related to morphological ally, the overall protein profile has never been alterations in the cytoskeleton, kinetoplast, and assessed and, considering that trypanosomatids paraflagellar rod of the host cell (Freymuller and expression is post-transcriptionally regulated, pro- Camargo 1981; Gadelha et al. 2005; Votypka´ et al. tein analysis is of outmost relevance (Brunoro et al. 2014). 2015; Clayton and Shapira 2007; Parodi-Talice The endosymbiont-trypanosomatid interaction et al. 2004). Here, we applied shotgun proteomics is characterized by intense metabolic exchange to compare endosymbiont-bearing (wild type) and (Alfieri and Camargo 1982; Camargo and endosymbiont-free (aposymbiotic) strains of S. culi- Freymuller 1977; Chang et al. 1975; Chang and cis, aiming at a better understanding of this intricate Trager 1974), which has been recently character- association. ized at genomic level (Alves et al. 2011, 2013a; Klein et al. 2013; Korenˇ y´ et al. 2010; Motta et al. 2013; Votypka´ et al. 2014). In spite of considerable Results genome reduction in the bacterium, it maintains genes responsible for the biosynthesis of com- Ultrastructural and Phylogenetic Analyses pounds essential for the host, either providing of S. culicis Wild Type (WT) and precursor molecules or complementing indispens- Aposymbiotic (Apo) Strains able biosynthetic pathways, such as those for amino acids, vitamins, cofactors, lipids, and the Inspection of the axenic cultures of each strain of S. purine/pyrimidine (Alves et al., 2013a, b; Azevedo- culicis by electron microscopy reinforced the pres- Martins et al.
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