Development of a Toolbox to Dissect Host-Endosymbiont Interactions And
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Identification and Phylogenetic Analysis of Heme Synthesis Genes in Trypanosomatids and Their Bacterial Endosymbionts
Identification and Phylogenetic Analysis of Heme Synthesis Genes in Trypanosomatids and Their Bacterial Endosymbionts Joa˜o M. P. Alves1*, Logan Voegtly1, Andrey V. Matveyev1, Ana M. Lara1, Fla´via Maia da Silva2, Myrna G. Serrano1, Gregory A. Buck1, Marta M. G. Teixeira2, Erney P. Camargo2 1 Department of Microbiology and Immunology and the Center for the Study of Biological Complexity, Virginia Commonwealth University, Richmond, Virginia, United States of America, 2 Department of Parasitology, ICB, University of Sa˜o Paulo, Sa˜o Paulo, Brazil Abstract It has been known for decades that some insect-infecting trypanosomatids can survive in culture without heme supplementation while others cannot, and that this capability is associated with the presence of a betaproteobacterial endosymbiont in the flagellate’s cytoplasm. However, the specific mechanisms involved in this process remained obscure. In this work, we sequence and phylogenetically analyze the heme pathway genes from the symbionts and from their hosts, as well as from a number of heme synthesis-deficient Kinetoplastida. Our results show that the enzymes responsible for synthesis of heme are encoded on the symbiont genomes and produced in close cooperation with the flagellate host. Our evidence suggests that this synergistic relationship is the end result of a history of extensive gene loss and multiple lateral gene transfer events in different branches of the phylogeny of the Trypanosomatidae. Citation: Alves JMP, Voegtly L, Matveyev AV, Lara AM, da Silva FM, et al. (2011) Identification and Phylogenetic Analysis of Heme Synthesis Genes in Trypanosomatids and Their Bacterial Endosymbionts. PLoS ONE 6(8): e23518. doi:10.1371/journal.pone.0023518 Editor: Purification Lopez-Garcia, Universite´ Paris Sud, France Received May 20, 2011; Accepted July 19, 2011; Published August 10, 2011 Copyright: ß 2011 Alves et al. -
Non-Leishmania Parasite in Fatal Visceral Leishmaniasis–Like Disease, Brazil
DISPATCHES Non-Leishmania Parasite in Fatal Visceral Leishmaniasis–Like Disease, Brazil Sandra R. Maruyama,1 Alynne K.M. de Santana,1,2 performed whole-genome sequencing of 2 clinical isolates Nayore T. Takamiya, Talita Y. Takahashi, from a patient with a fatal illness with clinical characteris- Luana A. Rogerio, Caio A.B. Oliveira, tics similar to those of VL. Cristiane M. Milanezi, Viviane A. Trombela, Angela K. Cruz, Amélia R. Jesus, The Study Aline S. Barreto, Angela M. da Silva, During 2011–2012, we characterized 2 parasite strains, LVH60 Roque P. Almeida,3 José M. Ribeiro,3 João S. Silva3 and LVH60a, isolated from an HIV-negative man when he was 64 years old and 65 years old (Table; Appendix, https:// Through whole-genome sequencing analysis, we identified wwwnc.cdc.gov/EID/article/25/11/18-1548-App1.pdf). non-Leishmania parasites isolated from a man with a fatal Treatment-refractory VL-like disease developed in the man; visceral leishmaniasis–like illness in Brazil. The parasites signs and symptoms consisted of weight loss, fever, anemia, infected mice and reproduced the patient’s clinical mani- festations. Molecular epidemiologic studies are needed to low leukocyte and platelet counts, and severe liver and spleen ascertain whether a new infectious disease is emerging that enlargements. VL was confirmed by light microscopic exami- can be confused with leishmaniasis. nation of amastigotes in bone marrow aspirates and promas- tigotes in culture upon parasite isolation and by positive rK39 serologic test results. Three courses of liposomal amphotericin eishmaniases are caused by ≈20 Leishmania species B resulted in no response. -
Recent Advances in Trypanosomatid Research: Genome Organization, Expression, Metabolism, Taxonomy and Evolution
Parasitology Recent advances in trypanosomatid research: genome organization, expression, metabolism, cambridge.org/par taxonomy and evolution 1 2 3,4 5,6 Review Dmitri A. Maslov , Fred R. Opperdoes , Alexei Y. Kostygov , Hassan Hashimi , Julius Lukeš5,6 and Vyacheslav Yurchenko3,5,7 Cite this article: Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V 1Department of Molecular, Cell and Systems Biology, University of California – Riverside, Riverside, California, USA; (2018). Recent advances in trypanosomatid 2de Duve Institute, Université Catholique de Louvain, Brussels, Belgium; 3Life Science Research Centre, Faculty of research: genome organization, expression, 4 metabolism, taxonomy and evolution. Science, University of Ostrava, Ostrava, Czech Republic; Zoological Institute of the Russian Academy of Sciences, 5 Parasitology 1–27. https://doi.org/10.1017/ St. Petersburg, Russia; Biology Centre, Institute of Parasitology, Czech Academy of Sciences, České Budejovice 6 S0031182018000951 (Budweis), Czech Republic; University of South Bohemia, Faculty of Sciences, České Budejovice (Budweis), Czech Republic and 7Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov Received: 30 January 2018 University, Moscow, Russia Revised: 23 April 2018 Accepted: 23 April 2018 Abstract Key words: Unicellular flagellates of the family Trypanosomatidae are obligatory parasites of inverte- Gene exchange; kinetoplast; metabolism; molecular and cell biology; taxonomy; brates, vertebrates and plants. Dixenous species are aetiological agents of a number of diseases trypanosomatidae in humans, domestic animals and plants. Their monoxenous relatives are restricted to insects. Because of the high biological diversity, adaptability to dramatically different environmental Author for correspondence: conditions, and omnipresence, these protists have major impact on all biotic communities Vyacheslav Yurchenko, E-mail: vyacheslav. -
A Global Analysis of Enzyme Compartmentalization to Glycosomes
pathogens Article A Global Analysis of Enzyme Compartmentalization to Glycosomes Hina Durrani 1, Marshall Hampton 2 , Jon N. Rumbley 3 and Sara L. Zimmer 1,* 1 Department of Biomedical Sciences, University of Minnesota Medical School, Duluth Campus, Duluth, MN 55812, USA; [email protected] 2 Mathematics & Statistics Department, University of Minnesota Duluth, Duluth, MN 55812, USA; [email protected] 3 College of Pharmacy, University of Minnesota, Duluth Campus, Duluth, MN 55812, USA; [email protected] * Correspondence: [email protected] Received: 25 March 2020; Accepted: 9 April 2020; Published: 12 April 2020 Abstract: In kinetoplastids, the first seven steps of glycolysis are compartmentalized into a glycosome along with parts of other metabolic pathways. This organelle shares a common ancestor with the better-understood eukaryotic peroxisome. Much of our understanding of the emergence, evolution, and maintenance of glycosomes is limited to explorations of the dixenous parasites, including the enzymatic contents of the organelle. Our objective was to determine the extent that we could leverage existing studies in model kinetoplastids to determine the composition of glycosomes in species lacking evidence of experimental localization. These include diverse monoxenous species and dixenous species with very different hosts. For many of these, genome or transcriptome sequences are available. Our approach initiated with a meta-analysis of existing studies to generate a subset of enzymes with highest evidence of glycosome localization. From this dataset we extracted the best possible glycosome signal peptide identification scheme for in silico identification of glycosomal proteins from any kinetoplastid species. Validation suggested that a high glycosome localization score from our algorithm would be indicative of a glycosomal protein. -
Importance of Angomonas Deanei KAP4 for Kdna
www.nature.com/scientificreports OPEN Importance of Angomonas deanei KAP4 for kDNA arrangement, cell division and maintenance of the host‑bacterium relationship Camila Silva Gonçalves1,2,5, Carolina Moura Costa Catta‑Preta3,5, Bruno Repolês4, Jeremy C. Mottram3, Wanderley De Souza1,2, Carlos Renato Machado4* & Maria Cristina M. Motta1,2* Angomonas deanei coevolves in a mutualistic relationship with a symbiotic bacterium that divides in synchronicity with other host cell structures. Trypanosomatid mitochondrial DNA is contained in the kinetoplast and is composed of thousands of interlocked DNA circles (kDNA). The arrangement of kDNA is related to the presence of histone‑like proteins, known as KAPs (kinetoplast‑associated proteins), that neutralize the negatively charged kDNA, thereby afecting the activity of mitochondrial enzymes involved in replication, transcription and repair. In this study, CRISPR‑Cas9 was used to delete both alleles of the A. deanei KAP4 gene. Gene‑defcient mutants exhibited high compaction of the kDNA network and displayed atypical phenotypes, such as the appearance of a flamentous symbionts, cells containing two nuclei and one kinetoplast, and division blocks. Treatment with cisplatin and UV showed that Δkap4 null mutants were not more sensitive to DNA damage and repair than wild‑type cells. Notably, lesions caused by these genotoxic agents in the mitochondrial DNA could be repaired, suggesting that the kDNA in the kinetoplast of trypanosomatids has unique repair mechanisms. Taken together, our data indicate that although KAP4 is not an essential protein, it plays important roles in kDNA arrangement and replication, as well as in the maintenance of symbiosis. Te kinetoplast contains the mitochondrial DNA (kDNA) of trypanosomatids, which is arranged in a network of several thousand minicircles categorized into diferent classes and several dozen maxicircles that are virtually identical. -
Trypanosomatids Are Much More Than Just Trypanosomes: Clues from The
Review Trypanosomatids Are Much More than Just Trypanosomes: Clues from the Expanded Family Tree 1,2, 1,3 1,2 4 1,5 Julius Lukeš, * Anzhelika Butenko, Hassan Hashimi, Dmitri A. Maslov, Jan Votýpka, and 1,3 Vyacheslav Yurchenko Trypanosomes and leishmanias are widely known parasites of humans. How- Highlights ever, they are just two out of several phylogenetic lineages that constitute the Dixenous trypanosomatids, such as the human Trypanosoma parasites, family Trypanosomatidae. Although dixeny – the ability to infect two hosts – is a infect both insects and vertebrates. derived trait of vertebrate-infecting parasites, the majority of trypanosomatids Yet phylogenetic analyses have revealed that these are the exception, are monoxenous. Like their common ancestor, the monoxenous Trypanoso- and that insect-infecting monoxenous matidae are mostly parasites or commensals of insects. This review covers lineages are both abundant and recent advances in the study of insect trypanosomatids, highlighting their diverse. diversity as well as genetic, morphological and biochemical complexity, which, Globally, over 10% of true bugs and until recently, was underappreciated. The investigation of insect trypanoso- flies are infected with monoxenous try- matids is providing an important foundation for understanding the origin and panosomatids, whereas other insect groups are infected much less fre- evolution of parasitism, including colonization of vertebrates and the appear- quently. Some trypanosomatids are ance of human pathogens. confined to a single host species, whereas others parasitize a wide spec- trum of hosts. One Host or Two? Lifestyles of the Trypanosomatidae All members of the family Trypanosomatidae are obligatory parasites and include the iconic Many trypanosomatids are themselves pathogens responsible for African sleeping sickness, Chagas’ disease and leishmaniases. -
Predicting the Proteins of Angomonas Deanei, Strigomonas Culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family Maria Cristina Machado Motta1, Allan Cezar de Azevedo Martins1, Silvana Sant’Anna de Souza1,2, Carolina Moura Costa Catta-Preta1, Rosane Silva2, Cecilia Coimbra Klein3,4,5, Luiz Gonzaga Paula de Almeida3, Oberdan de Lima Cunha3, Luciane Prioli Ciapina3, Marcelo Brocchi6, Ana Cristina Colabardini7, Bruna de Araujo Lima6, Carlos Renato Machado9,Ce´lia Maria de Almeida Soares10, Christian Macagnan Probst11,12, Claudia Beatriz Afonso de Menezes13, Claudia Elizabeth Thompson3, Daniella Castanheira Bartholomeu14, Daniela Fiori Gradia11, Daniela Parada Pavoni12, Edmundo C. Grisard15, Fabiana Fantinatti-Garboggini13, Fabricio Klerynton Marchini12, Gabriela Fla´via Rodrigues-Luiz14, Glauber Wagner15, Gustavo Henrique Goldman7, Juliana Lopes Rangel Fietto16, Maria Carolina Elias17, Maria Helena S. Goldman18, Marie-France Sagot4,5, Maristela Pereira10, Patrı´cia H. Stoco15, Rondon Pessoa de Mendonc¸a-Neto9, Santuza Maria Ribeiro Teixeira9, Talles Eduardo Ferreira Maciel16, Tiago Antoˆ nio de Oliveira Mendes14, Tura´nP.U¨ rme´nyi2, Wanderley de Souza1, Sergio Schenkman19*, Ana Tereza Ribeiro de Vasconcelos3* 1 Laborato´rio de Ultraestrutura Celular Hertha Meyer, Instituto de Biofı´sica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil, 2 Laborato´rio de Metabolismo Macromolecular Firmino Torres de Castro, Instituto de Biofı´sica Carlos Chagas Filho, -
Evolutionary Analyses of Myosin Genes in Trypanosomatids Show A
www.nature.com/scientificreports OPEN Evolutionary analyses of myosin genes in trypanosomatids show a history of expansion, secondary Received: 15 September 2017 Accepted: 18 December 2017 losses and neofunctionalization Published: xx xx xxxx Denise Andréa Silva de Souza1,2, Daniela Parada Pavoni1,2, Marco Aurélio Krieger1,2,3 & Adriana Ludwig1,3 Myosins are motor proteins that comprise a large and diversifed family important for a broad range of functions. Two myosin classes, I and XIII, were previously assigned in Trypanosomatids, based mainly on the studies of Trypanosoma cruzi, T. brucei and Leishmania major, and important human pathogenic species; seven orphan myosins were identifed in T. cruzi. Our results show that the great variety of T. cruzi myosins is also present in some closely related species and in Bodo saltans, a member of an early divergent branch of Kinetoplastida. Therefore, these myosins should no longer be considered “orphans”. We proposed the classifcation of a kinetoplastid-specifc myosin group into a new class, XXXVI. Moreover, our phylogenetic data suggest that a great repertoire of myosin genes was present in the last common ancestor of trypanosomatids and B. saltans, mainly resulting from several gene duplications. These genes have since been predominantly maintained in synteny in some species, and secondary losses explain the current distribution. We also found two interesting genes that were clearly derived from myosin genes, demonstrating that possible redundant or useless genes, instead of simply being lost, can serve as raw material for the evolution of new genes and functions. Myosins are important eukaryotic molecular motor proteins that bind actin flaments and are dependent of ATP hydrolysis1. -
Genomics of Trypanosomatidae: Where We Stand and What Needs to Be Done?
pathogens Review Genomics of Trypanosomatidae: Where We Stand and What Needs to Be Done? Vyacheslav Yurchenko 1,2,* , Anzhelika Butenko 1,3 and Alexei Y. Kostygov 1,4,* 1 Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic; [email protected] 2 Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, 119435 Moscow, Russia 3 Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 Ceskˇ é Budˇejovice, Czech Republic 4 Zoological Institute of the Russian Academy of Sciences, 190121 St. Petersburg, Russia * Correspondence: [email protected] (V.Y.); [email protected] (A.Y.K.) Abstract: Trypanosomatids are easy to cultivate and they are (in many cases) amenable to genetic manipulation. Genome sequencing has become a standard tool routinely used in the study of these flagellates. In this review, we summarize the current state of the field and our vision of what needs to be done in order to achieve a more comprehensive picture of trypanosomatid evolution. This will also help to illuminate the lineage-specific proteins and pathways, which can be used as potential targets in treating diseases caused by these parasites. Keywords: trypanosomatids; next-generation sequencing; genomics Citation: Yurchenko, V.; Butenko, A.; Kostygov, A.Y. Genomics of 1. Introduction Trypanosomatidae: Where We Stand The flagellates of the family Trypanosomatidae represent one of the most evolu- and What Needs to Be tionarily successful groups of parasitic protists, adapted to an extremely wide range of Done? Pathogens 2021, 10, 1124. hosts—from various animals (mainly insects and vertebrates) to flowering plants and even https://doi.org/10.3390/pathogens ciliates. -
Symbiont Modulates Expression of Specific Gene Categories in Angomonas Deanei
686 Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 111(11): 686-691, November 2016 Symbiont modulates expression of specific gene categories in Angomonas deanei Luciana Loureiro Penha, Luísa Hoffmann, Silvanna Sant’Anna de Souza, Allan Cézar de Azevedo Martins, Thayane Bottaro, Francisco Prosdocimi, Débora Souza Faffe, Maria Cristina Machado Motta, Turán Péter Ürményi, Rosane Silva/+ Universidade Federal do Rio de Janeiro, Instituto de Biofísica Carlos Chagas Filho, Rio de Janeiro, RJ, Brasil Trypanosomatids are parasites that cause disease in humans, animals, and plants. Most are non-pathogenic and some harbor a symbiotic bacterium. Endosymbiosis is part of the evolutionary process of vital cell functions such as respiration and photosynthesis. Angomonas deanei is an example of a symbiont-containing trypanosomatid. In this paper, we sought to investigate how symbionts influence host cells by characterising and comparing the transcriptomes of the symbiont-containing A. deanei (wild type) and the symbiont-free aposymbiotic strains. The comparison revealed that the presence of the symbiont modulates several differentially expressed genes. Empirical analysis of differential gene expression showed that 216 of the 7625 modulated genes were significantly changed. Finally, gene set enrichment analysis revealed that the largest categories of genes that downregulated in the absence of the symbiont were those in- volved in oxidation-reduction process, ATP hydrolysis coupled proton transport and glycolysis. In contrast, among the upregulated gene categories were those involved in proteolysis, microtubule-based movement, and cellular metabolic process. Our results provide valuable information for dissecting the mechanism of endosymbiosis in A. deanei. Key words: trypanosomatid RNA-seq - gene expression - aposymbiotic strain - endosymbiosis An important part of eukaryotic cell evolution was was generated by chloramphenicol treatment and thus the acquisition of new organelles through endosymbio- represents a valuable tool to study how the symbiont in- sis. -
AQPX-Cluster Aquaporins and Aquaglyceroporins Are
ARTICLE https://doi.org/10.1038/s42003-021-02472-9 OPEN AQPX-cluster aquaporins and aquaglyceroporins are asymmetrically distributed in trypanosomes ✉ ✉ Fiorella Carla Tesan 1,2, Ramiro Lorenzo 3, Karina Alleva 1,2,4 & Ana Romina Fox 3,4 Major Intrinsic Proteins (MIPs) are membrane channels that permeate water and other small solutes. Some trypanosomatid MIPs mediate the uptake of antiparasitic compounds, placing them as potential drug targets. However, a thorough study of the diversity of these channels is still missing. Here we place trypanosomatid channels in the sequence-function space of the large MIP superfamily through a sequence similarity network. This analysis exposes that trypanosomatid aquaporins integrate a distant cluster from the currently defined MIP 1234567890():,; families, here named aquaporin X (AQPX). Our phylogenetic analyses reveal that trypano- somatid MIPs distribute exclusively between aquaglyceroporin (GLP) and AQPX, being the AQPX family expanded in the Metakinetoplastina common ancestor before the origin of the parasitic order Trypanosomatida. Synteny analysis shows how African trypanosomes spe- cifically lost AQPXs, whereas American trypanosomes specifically lost GLPs. AQPXs diverge from already described MIPs on crucial residues. Together, our results expose the diversity of trypanosomatid MIPs and will aid further functional, structural, and physiological research needed to face the potentiality of the AQPXs as gateways for trypanocidal drugs. 1 Universidad de Buenos Aires, Facultad de Farmacia y Bioquímica, Departamento de Fisicomatemática, Cátedra de Física, Buenos Aires, Argentina. 2 CONICET-Universidad de Buenos Aires, Instituto de Química y Fisicoquímica Biológicas (IQUIFIB), Buenos Aires, Argentina. 3 Laboratorio de Farmacología, Centro de Investigación Veterinaria de Tandil (CIVETAN), (CONICET-CICPBA-UNCPBA) Facultad de Ciencias Veterinarias, Universidad Nacional del Centro ✉ de la Provincia de Buenos Aires, Tandil, Argentina. -
Trypanosomatids Are Much More Than Just Trypanosomes: Clues from the Expanded Family Tree
UC Riverside UC Riverside Previously Published Works Title Trypanosomatids Are Much More than Just Trypanosomes: Clues from the Expanded Family Tree. Permalink https://escholarship.org/uc/item/89h481p3 Journal Trends in parasitology, 34(6) ISSN 1471-4922 Authors Lukeš, Julius Butenko, Anzhelika Hashimi, Hassan et al. Publication Date 2018-06-01 DOI 10.1016/j.pt.2018.03.002 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Review Trypanosomatids Are Much More than Just Trypanosomes: Clues from the Expanded Family Tree 1,2, 1,3 1,2 4 1,5 Julius Lukeš, * Anzhelika Butenko, Hassan Hashimi, Dmitri A. Maslov, Jan Votýpka, and 1,3 Vyacheslav Yurchenko Trypanosomes and leishmanias are widely known parasites of humans. How- Highlights ever, they are just two out of several phylogenetic lineages that constitute the Dixenous trypanosomatids, such as the human Trypanosoma parasites, family Trypanosomatidae. Although dixeny – the ability to infect two hosts – is a infect both insects and vertebrates. derived trait of vertebrate-infecting parasites, the majority of trypanosomatids Yet phylogenetic analyses have revealed that these are the exception, are monoxenous. Like their common ancestor, the monoxenous Trypanoso- and that insect-infecting monoxenous matidae are mostly parasites or commensals of insects. This review covers lineages are both abundant and recent advances in the study of insect trypanosomatids, highlighting their diverse. diversity as well as genetic, morphological and biochemical complexity, which, Globally, over 10% of true bugs and until recently, was underappreciated. The investigation of insect trypanoso- flies are infected with monoxenous try- matids is providing an important foundation for understanding the origin and panosomatids, whereas other insect groups are infected much less fre- evolution of parasitism, including colonization of vertebrates and the appear- quently.