Research

13 pages, 2570 KiB

Open AccessArticle

Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids Angomonas spp.

by Tomáš Skalický, João M. P. Alves, Anderson C. Morais, Jana Režnarová, Anzhelika Butenko, Julius Lukeš, Myrna G. Serrano, Gregory A. Buck, Marta M. G. Teixeira, Erney P. Camargo, Mandy Sanders, James A. Cotton, Vyacheslav Yurchenko and Alexei Y. Kostygov

Pathogens 2021, 10(6), 702; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10060702 - 04 Jun 2021

Cited by 2 | Viewed by 3117

Abstract

Trypanosomatids of the subfamily Strigomonadinae bear permanent intracellular bacterial symbionts acquired by the common ancestor of these flagellates. However, the cospeciation pattern inherent to such relationships was revealed to be broken upon the description of Angomonas ambiguus, which is sister to A. [...] Read more.

Trypanosomatids of the subfamily Strigomonadinae bear permanent intracellular bacterial symbionts acquired by the common ancestor of these flagellates. However, the cospeciation pattern inherent to such relationships was revealed to be broken upon the description of Angomonas ambiguus, which is sister to A. desouzai, but bears an endosymbiont genetically close to that of A. deanei. Based on phylogenetic inferences, it was proposed that the bacterium from A. deanei had been horizontally transferred to A. ambiguus. Here, we sequenced the bacterial genomes from two A. ambiguus isolates, including a new one from Papua New Guinea, and compared them with the published genome of the A. deanei endosymbiont, revealing differences below the interspecific level. Our phylogenetic analyses confirmed that the endosymbionts of A. ambiguus were obtained from A. deanei and, in addition, demonstrated that this occurred more than once. We propose that coinfection of the same blowfly host and the phylogenetic relatedness of the trypanosomatids facilitate such transitions, whereas the drastic difference in the occurrence of the two trypanosomatid species determines the observed direction of this process. This phenomenon is analogous to organelle (mitochondrion/plastid) capture described in multicellular organisms and, thereafter, we name it endosymbiont capture. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

12 pages, 683 KiB

Open AccessArticle

The Remarkable Metabolism of Vickermania ingenoplastis: Genomic Predictions

by Fred R. Opperdoes, Anzhelika Butenko, Alexandra Zakharova, Evgeny S. Gerasimov, Sara L. Zimmer, Julius Lukeš and Vyacheslav Yurchenko

Pathogens 2021, 10(1), 68; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10010068 - 14 Jan 2021

Cited by 8 | Viewed by 2658

Abstract

A recently redescribed two-flagellar trypanosomatid Vickermania ingenoplastis is insensitive to the classical inhibitors of respiration and thrives under anaerobic conditions. Using genomic and transcriptomic data, we analyzed its genes of the core metabolism and documented that subunits of the mitochondrial respiratory complexes III [...] Read more.

A recently redescribed two-flagellar trypanosomatid Vickermania ingenoplastis is insensitive to the classical inhibitors of respiration and thrives under anaerobic conditions. Using genomic and transcriptomic data, we analyzed its genes of the core metabolism and documented that subunits of the mitochondrial respiratory complexes III and IV are ablated, while those of complexes I, II, and V are all present, along with an alternative oxidase. This explains the previously reported conversion of glucose to acetate and succinate by aerobic fermentation. Glycolytic pyruvate is metabolized to acetate and ethanol by pyruvate dismutation, whereby a unique type of alcohol dehydrogenase (shared only with Phytomonas spp.) processes an excess of reducing equivalents formed under anaerobic conditions, leading to the formation of ethanol. Succinate (formed to maintain the glycosomal redox balance) is converted to propionate by a cyclic process involving three enzymes of the mitochondrial methyl-malonyl-CoA pathway, via a cyclic process, which results in the formation of additional ATP. The unusual structure of the V. ingenoplastis genome and its similarity with that of Phytomonas spp. imply their relatedness or convergent evolution. Nevertheless, a critical difference between these two trypanosomatids is that the former has significantly increased its genome size by gene duplications, while the latter streamlined its genome. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

12 pages, 1235 KiB

Open AccessArticle

Frequent Recombination Events in Leishmania donovani: Mining Population Data

by Igor B. Rogozin, Arzuv Charyyeva, Ivan A. Sidorenko, Vladimir N. Babenko and Vyacheslav Yurchenko

Pathogens 2020, 9(7), 572; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9070572 - 15 Jul 2020

Cited by 5 | Viewed by 2229

Abstract

The Leishmania donovani species complex consists of all L. donovani and L. infantum strains mainly responsible for visceral leishmaniasis (VL). It was suggested that genome rearrangements in Leishmania spp. occur very often, thus enabling parasites to adapt to the different environmental conditions. Some [...] Read more.

The Leishmania donovani species complex consists of all L. donovani and L. infantum strains mainly responsible for visceral leishmaniasis (VL). It was suggested that genome rearrangements in Leishmania spp. occur very often, thus enabling parasites to adapt to the different environmental conditions. Some of these rearrangements may be directly linked to the virulence or explain the reduced efficacy of antimonial drugs in some isolates. In the current study, we focused on a large-scale analysis of putative gene conversion events using publicly available datasets. Previous population study of L. donovani suggested that population variability of L. donovani is relatively low, however the authors used masking procedures and strict read selection criteria. We decided to re-analyze DNA-seq data without masking sequences, because we were interested in the most dynamic fraction of the genome. The majority of samples have an excess of putative gene conversion/recombination events in the noncoding regions, however we found an overall excess of putative intrachromosomal gene conversion/recombination in the protein coding genes, compared to putative interchromosomal gene conversion/recombination events. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

16 pages, 3419 KiB

Open AccessArticle

Catalase and Ascorbate Peroxidase in Euglenozoan Protists

by Ingrid Škodová-Sveráková, Kristína Záhonová, Barbora Bučková, Zoltán Füssy, Vyacheslav Yurchenko and Julius Lukeš

Pathogens 2020, 9(4), 317; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9040317 - 24 Apr 2020

Cited by 11 | Viewed by 3461

Abstract

In this work, we studied the biochemical properties and evolutionary histories of catalase (CAT) and ascorbate peroxidase (APX), two central enzymes of reactive oxygen species detoxification, across the highly diverse clade Eugenozoa. This clade encompasses free-living phototrophic and heterotrophic flagellates, as well as [...] Read more.

In this work, we studied the biochemical properties and evolutionary histories of catalase (CAT) and ascorbate peroxidase (APX), two central enzymes of reactive oxygen species detoxification, across the highly diverse clade Eugenozoa. This clade encompasses free-living phototrophic and heterotrophic flagellates, as well as obligate parasites of insects, vertebrates, and plants. We present evidence of several independent acquisitions of CAT by horizontal gene transfers and evolutionary novelties associated with the APX presence. We posit that Euglenozoa recruit these detoxifying enzymes for specific molecular tasks, such as photosynthesis in euglenids and membrane-bound peroxidase activity in kinetoplastids and some diplonemids. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

19 pages, 1825 KiB

Open AccessArticle

A Global Analysis of Enzyme Compartmentalization to Glycosomes

by Hina Durrani, Marshall Hampton, Jon N. Rumbley and Sara L. Zimmer

Pathogens 2020, 9(4), 281; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9040281 - 12 Apr 2020

Cited by 7 | Viewed by 2769

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 [...] Read more.

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. We found that while metabolic pathways were consistently represented across kinetoplastids, individual proteins within those pathways may not universally exhibit evidence of glycosome localization. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Graphical abstract

16 pages, 3857 KiB

Open AccessArticle

Inventory and Evolution of Mitochondrion-localized Family A DNA Polymerases in Euglenozoa

by Ryo Harada, Yoshihisa Hirakawa, Akinori Yabuki, Yuichiro Kashiyama, Moe Maruyama, Ryo Onuma, Petr Soukal, Shinya Miyagishima, Vladimír Hampl, Goro Tanifuji and Yuji Inagaki

Pathogens 2020, 9(4), 257; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9040257 - 01 Apr 2020

Cited by 8 | Viewed by 3448

Abstract

The order Trypanosomatida has been well studied due to its pathogenicity and the unique biology of the mitochondrion. In Trypanosoma brucei, four DNA polymerases, namely PolIA, PolIB, PolIC, and PolID, related to bacterial DNA polymerase I (PolI), were shown to be localized [...] Read more.

The order Trypanosomatida has been well studied due to its pathogenicity and the unique biology of the mitochondrion. In Trypanosoma brucei, four DNA polymerases, namely PolIA, PolIB, PolIC, and PolID, related to bacterial DNA polymerase I (PolI), were shown to be localized in mitochondria experimentally. These mitochondrion-localized DNA polymerases are phylogenetically distinct from other family A DNA polymerases, such as bacterial PolI, DNA polymerase gamma (Polγ) in human and yeasts, “plant and protist organellar DNA polymerase (POP)” in diverse eukaryotes. However, the diversity of mitochondrion-localized DNA polymerases in Euglenozoa other than Trypanosomatida is poorly understood. In this study, we discovered putative mitochondrion-localized DNA polymerases in broad members of three major classes of Euglenozoa—Kinetoplastea, Diplonemea, and Euglenida—to explore the origin and evolution of trypanosomatid PolIA-D. We unveiled distinct inventories of mitochondrion-localized DNA polymerases in the three classes: (1) PolIA is ubiquitous across the three euglenozoan classes, (2) PolIB, C, and D are restricted in kinetoplastids, (3) new types of mitochondrion-localized DNA polymerases were identified in a prokinetoplastid and diplonemids, and (4) evolutionarily distinct types of POP were found in euglenids. We finally propose scenarios to explain the inventories of mitochondrion-localized DNA polymerases in Kinetoplastea, Diplonemea, and Euglenida. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

17 pages, 17460 KiB

Open AccessArticle

Common Structural Patterns in the Maxicircle Divergent Region of Trypanosomatidae

by Evgeny S. Gerasimov, Ksenia A. Zamyatnina, Nadezda S. Matveeva, Yulia A. Rudenskaya, Natalya Kraeva, Alexander A. Kolesnikov and Vyacheslav Yurchenko

Pathogens 2020, 9(2), 100; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9020100 - 05 Feb 2020

Cited by 15 | Viewed by 2746

Abstract

Maxicircles of all kinetoplastid flagellates are functional analogs of mitochondrial genome of other eukaryotes. They consist of two distinct parts, called the coding region and the divergent region (DR). The DR is composed of highly repetitive sequences and, as such, remains the least [...] Read more.

Maxicircles of all kinetoplastid flagellates are functional analogs of mitochondrial genome of other eukaryotes. They consist of two distinct parts, called the coding region and the divergent region (DR). The DR is composed of highly repetitive sequences and, as such, remains the least explored segment of a trypanosomatid genome. It is extremely difficult to sequence and assemble, that is why very few full length maxicircle sequences were available until now. Using PacBio data, we assembled 17 complete maxicircles from different species of trypanosomatids. Here we present their large-scale comparative analysis and describe common patterns of DR organization in trypanosomatids. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

17 pages, 3991 KiB

Open AccessArticle

Evolutionary Insight into the Trypanosomatidae Using Alignment-Free Phylogenomics of the Kinetoplast

by Alexa Kaufer, Damien Stark and John Ellis

Pathogens 2019, 8(3), 157; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens8030157 - 18 Sep 2019

Cited by 10 | Viewed by 4615

Abstract

Advancements in next-generation sequencing techniques have led to a substantial increase in the genomic information available for analyses in evolutionary biology. As such, this data requires the exponential growth in bioinformatic methods and expertise required to understand such vast quantities of genomic data. [...] Read more.

Advancements in next-generation sequencing techniques have led to a substantial increase in the genomic information available for analyses in evolutionary biology. As such, this data requires the exponential growth in bioinformatic methods and expertise required to understand such vast quantities of genomic data. Alignment-free phylogenomics offer an alternative approach for large-scale analyses that may have the potential to address these challenges. The evolutionary relationships between various species within the trypanosomatid family, specifically members belonging to the genera Leishmania and Trypanosoma have been extensively studies over the last 30 years. However, there is a need for a more exhaustive analysis of the Trypanosomatidae, summarising the evolutionary patterns amongst the entire family of these important protists. The mitochondrial DNA of the trypanosomatids, better known as the kinetoplast, represents a valuable taxonomic marker given its unique presence across all kinetoplastid protozoans. The aim of this study was to validate the reliability and robustness of alignment-free approaches for phylogenomic analyses and its applicability to reconstruct the evolutionary relationships between the trypanosomatid family. In the present study, alignment-free analyses demonstrated the strength of these methods, particularly when dealing with large datasets compared to the traditional phylogenetic approaches. We present a maxicircle genome phylogeny of 46 species spanning the trypanosomatid family, demonstrating the superiority of the maxicircle for the analysis and taxonomic resolution of the Trypanosomatidae. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

Review

Jump to: Research, Other

15 pages, 724 KiB

Open AccessReview

Genomics of Trypanosomatidae: Where We Stand and What Needs to Be Done?

by Vyacheslav Yurchenko, Anzhelika Butenko and Alexei Y. Kostygov

Pathogens 2021, 10(9), 1124; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10091124 - 02 Sep 2021

Cited by 11 | Viewed by 3029

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

Other

Jump to: Research, Review

13 pages, 4219 KiB

Open AccessConcept Paper

Genomics and High-Resolution Typing Confirm Predominant Clonal Evolution Down to a Microevolutionary Scale in Trypanosoma cruzi

by Michel Tibayrenc and Francisco J. Ayala

Pathogens 2020, 9(5), 356; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens9050356 - 08 May 2020

Cited by 3 | Viewed by 2063

Abstract

Trypanosoma cruzi, the agent of Chagas disease, is a paradigmatic case of the predominant clonal evolution (PCE) model, which states that the impact of genetic recombination in pathogens’ natural populations is not sufficient to suppress a persistent phylogenetic signal at all evolutionary [...] Read more.

Trypanosoma cruzi, the agent of Chagas disease, is a paradigmatic case of the predominant clonal evolution (PCE) model, which states that the impact of genetic recombination in pathogens’ natural populations is not sufficient to suppress a persistent phylogenetic signal at all evolutionary scales. In spite of indications for occasional recombination and meiosis, recent genomics and high-resolution typing data in T. cruzi reject the counterproposal that PCE does not operate at lower evolutionary scales, within the evolutionary units (=near-clades) that subdivide the species. Evolutionary patterns in the agent of Chagas disease at micro- and macroevolutionary scales are strikingly similar (“Russian doll pattern”), suggesting gradual, rather than saltatory evolution. Full article

(This article belongs to the Special Issue Kinetoplastid Phylogenomics and Evolution)

► Show Figures

Figure 1

Journal Menu

Journal Browser

Kinetoplastid Phylogenomics and Evolution

Share This Special Issue

Special Issue Editors

Special Issue Information

Keywords

Published Papers (10 papers)

Research

Review

Other

Further Information

Guidelines

MDPI Initiatives

Follow MDPI