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The Current View on Apicomplexan Parasites: Structure, Function, Evolution

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Parasitology".

Deadline for manuscript submissions: closed (15 October 2023) | Viewed by 17821

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Special Issue Editor

Dr. Ferenc Orosz

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Guest Editor

Institute of Enzymology, Budapest, Hungary
Interests: cytoskeleton; apicomplexa; phylogenetics
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Apicomplexan parasites cause serious illnesses, including malaria, in humans and domestic animals. The namesake of this phylum is the apical complex, a structure composed of specific organelles and cytoskeletal elements. How parasitism depends on the specific structure of these protists is still a poorly understood area. The host-parasite interaction is influenced by a number of apicomplexan-specific macromolecules. Apicomplexans contain also the apicoplast, a relict chloroplast. Studying this organelle helps understanding how apicomplexan parasites evolved from their free-living ancestors. Thus, this phylum is an extremely interesting one from evolutionary point of view as well.

The aim of this volume is to provide a broad overview of the current state of apicomplexan research. Therefore, on the one hand, we expect review papers, and on the other hand, articles presenting current results, from all areas of the field. Articles about less popular species are especially welcome (e.g. gregarines) as well as phylogenetic works and structural studies.

Dr. Ferenc Orosz
Guest Editor

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Keywords

apicomplexans
apical complex
conoid
apicoplast
aconoidasida
conoidasida
gregarinasina
plasmodium
toxoplasma
host-pathogen interaction
phylogenetics
evolution

Published Papers (10 papers)

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Research

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14 pages, 3095 KiB

Open AccessArticle

Plasmodium chabaudi Merozoites Obtained through a Simpler Method Do Not Survive in Classically Activated Macrophages

by Pedro Souto Rodrigues, Milena de Farias Azeredo, Natália de Souza Almeida, Gisela Garcia Cabral Galaxe de Almeida, João Luiz Mendes Wanderley, Sergio Henrique Seabra and Renato Augusto DaMatta

Microorganisms 2024, 12(1), 105; https://doi.org/10.3390/microorganisms12010105 - 05 Jan 2024

Viewed by 806

Abstract

Malaria is caused by apicomplexan parasites of the Plasmodium genus. Plasmodium chabaudi is an excellent animal model for the study of human malaria caused by P. falciparum. Merozoites invade erythrocytes but are also found in other host cells including macrophages from the spleen and liver. Methodologies for obtaining merozoites usually involve treatment with protease inhibitors. However, merozoites obtained in this way may have their enzymatic profile altered and, therefore, are not ideal for cell-interaction assays. We report the obtainment of P. chabaudi merozoites naturally egressed from a synchronous erythrocyte population infected with schizonts forms. Merozoites had their infectivity and ultrastructure analyzed. Interaction assays were performed with mice erythrocytes and classically activated mice peritoneal macrophages, a very well-established classic model. Obtained merozoites were able to kill mice and efficiently infect erythrocytes. Interestingly, a lower merozoite:erythrocyte ratio resulted in a higher percentage of infected erythrocytes. We describe a simpler method for obtaining viable and infective merozoites. Classically activated macrophages killed merozoites, suggesting that these host cells may not serve as reservoirs for these parasites. These findings have implications for our understanding of P. chabaudi merozoite biology and may improve the comprehension of their host–parasite relationship. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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14 pages, 2867 KiB

Open AccessArticle

Changes in the Proliferation of the Neural Progenitor Cells of Adult Mice Chronically Infected with Toxoplasma gondii

by Verónica Anaya-Martínez, Jhony Anacleto-Santos, Ricardo Mondragón-Flores, Armando Zepeda-Rodríguez, Brenda Casarrubias-Tabarez, Teresa de Jesús López-Pérez, Mariana Citlalli de Alba-Alvarado, Cintli Martínez-Ortiz-de-Montellano, Elba Carrasco-Ramírez and Norma Rivera-Fernández

Microorganisms 2023, 11(11), 2671; https://doi.org/10.3390/microorganisms11112671 - 31 Oct 2023

Viewed by 983

Abstract

During Toxoplasma gondii chronic infection, certain internal factors that trigger the proliferation of neural progenitor cells (NPCs), such as brain inflammation, cell death, and changes in cytokine levels, are observed. NPCs give rise to neuronal cell types in the adult brain of some mammals. NPCs are capable of dividing and differentiating into a restricted repertoire of neuronal and glial cell types. In this study, the proliferation of NPCs was evaluated in CD-1 adult male mice chronically infected with the T. gondii ME49 strain. Histological brain sections from the infected mice were evaluated in order to observe T. gondii tissue cysts. Sagittal and coronal sections from the subventricular zone of the lateral ventricles and from the subgranular zone of the hippocampal dentate gyrus, as well as sagittal sections from the rostral migratory stream, were obtained from infected and non-infected mice previously injected with bromodeoxyuridine (BrdU). A flotation immunofluorescence technique was used to identify BrdU+ NPC. The scanning of BrdU+ cells was conducted using a confocal microscope, and the counting was performed with ImageJ^® software (version 1.48q). In all the evaluated zones from the infected mice, a significant proliferation of the NPCs was observed when compared with that of the control group. We concluded that chronic infection with T. gondii increased the proliferation of NPCs in the three evaluated zones. Regardless of the role these cells are playing, our results could be useful to better understand the pathogenesis of chronic toxoplasmosis. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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13 pages, 2405 KiB

Open AccessArticle

Phylogenetic Inferences Based on Distinct Molecular Markers Confirm a Novel Babesia Species (Babesia goianiaensis nov. sp.) in Capybaras (Hydrochoerus hydrochaeris) and Associated Ticks

by Felipe da Silva Krawczak, Ana Cláudia Calchi, Lucianne Cardoso Neves, Sarah Alves Dias, Bianca Barbara Fonseca da Silva, Warley Vieira de Freitas Paula, Luiza Gabriella Ferreira de Paula, Mariana Avelar Tavares, Gracielle Teles Pádua, Nicolas Jalowitzki de Lima, Ennya Rafaella Neves Cardoso, Daniel Graziani, Filipe Dantas-Torres and Marcos Rogério André

Microorganisms 2023, 11(8), 2022; https://doi.org/10.3390/microorganisms11082022 - 06 Aug 2023

Cited by 1 | Viewed by 1299

Abstract

Piroplasmids (order Piroplasmida) are a diverse group of tick-borne protozoa that may cause disease in animals and occasionally in humans. Novel Piroplasmida clades and species have been found in wild animals from Brazil based on the phylogenetic assessment of near-complete 18S rRNA, mitochondrial and heat-shock protein genes. For instance, a putative novel Babesia species has been detected in capybaras and Amblyomma ticks in three Brazilian states. The present work aimed to describe, using phylogenetic assessments based on distinct molecular markers, this novel Babesia species in capybaras and associated ticks (Amblyomma sculptum and Amblyomma dubitatum) sampled in Goiânia city, Goiás state, midwestern Brazil. While the phylogenetic analysis based on both near-complete 18S rRNA and hsp-70 genes positioned the sequences obtained from capybara blood samples into a new clade sister to the Babesia sensu stricto clade, the phylogenetic inference based on the COX-3 amino acid positioned the obtained sequences from capybara blood samples and A. sculptum ticks also into a clade sister to the Theileria sensu stricto clade, highlighting the inappropriateness of this marker inferring evolutionary relationships among piroplasmids. Pairwise distance analysis demonstrated that the divergence rates between the 18S rRNA sequences detected in capybaras and other Piroplasmida already described were very high and ranged from 9.4 to 12.9%. Genotype analysis based on the near-full 18S rRNA sequences of the Piroplasmida detected in capybaras and associated ticks demonstrated the occurrence of high genotype diversity at an intra-species level. In conclusion, phylogenetic analyses based on distinct molecular markers supported the description of Babesia goianiaensis nov. sp. in capybaras and associated Amblyomma ticks. Additionally, a novel phylogenetic clade, apart from the previously described ones, was described in the present study and contributed to untangling the complex evolutionary history of the Piroplasmida. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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14 pages, 4396 KiB

Open AccessArticle

Fluorescent Nanoparticle Uptake by Myzocytosis and Endocytosis in Colpodella sp. ATCC 50594

by Tobili Y. Sam-Yellowe, Mary M. Asraf, John W. Peterson and Hisashi Fujioka

Microorganisms 2023, 11(8), 1945; https://doi.org/10.3390/microorganisms11081945 - 29 Jul 2023

Cited by 1 | Viewed by 1010

Abstract

Colpodella sp. (ATCC 50594) is a free-living biflagellate predator closely related to pathogenic Apicomplexa such as Plasmodium, Cryptosporidium and Toxoplasma gondii. Colpodella sp. (ATCC 50594) obtain nutrients by preying on Parabodo caudatus using myzocytosis. The organization of the myzocytic apparatus and the mechanism of nutrient uptake into the posterior food vacuole of Colpodella species is unknown. In this study, we investigated myzocytosis using light and transmission electron microscopy. We investigated the uptake of 40 nm and 100 nm fluorescent nanoparticles and E. coli BioParticles by Colpodella sp. (ATCC 50594) in a diprotist culture. Transmission electron microscopy was used to investigate the morphology of the tubular tether formed during myzocytosis. E. coli BioParticles were taken up by P. caudatus but not by Colpodella sp. (ATCC 50594). Both protists took up the 100 nm and 40 nm beads, which were observed distributed in the cytoplasm of free unattached Colpodella sp. (ATCC 50594) trophozoites, and also in feeding Colpodella sp. (ATCC 50594) trophozoites and in the pre-cysts. Fragments of the nucleus and kinetoplast of P. caudatus and the nanoparticles were identified in the tubular tether being aspirated into the posterior food vacuole of Colpodella sp. (ATCC 50594). Unattached Colpodella sp. (ATCC 50594) endocytose nutrients from the culture medium independently from myzocytosis. The mechanisms of myzocytosis and endocytosis among Colpodella species may provide important insights into nutrient uptake among the pathogenic apicomplexans. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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15 pages, 1285 KiB

Open AccessArticle

Molecular Phylogenies of Leeches and Haemoparasites Infecting Freshwater Turtles in Aquatic Ecosystems of Northern Africa Suggest Phylogenetic Congruence between Placobdella costata Sensu Lato and Haemogregarina stepanowi Sensu Lato

by Olivier Verneau, Sirine Melliti, Latifa Kimdil, El Hassan El Mouden, Mohamed Sghaier Achouri and Rachid Rouag

Microorganisms 2023, 11(6), 1584; https://doi.org/10.3390/microorganisms11061584 - 15 Jun 2023

Cited by 2 | Viewed by 1449

Abstract

Haemogregarines are blood parasites with a life-cycle involving a vertebrate as the intermediate host and an invertebrate as the definitive host and vector. Extensive phylogenetic investigations based on 18S-rRNA gene sequences have shown that Haemogregarina stepanowi (Apicomplexa: Haemogregarinidae) is able to infest a large diversity of freshwater turtle species, including the European pond turtle Emys orbicularis, the Sicilian pond turtle Emys trinacris, the Caspian turtle Mauremys caspica, the Mediterranean pond turtle Mauremys leprosa, and the Western Caspian turtle Mauremys rivulata, among others. From the same molecular markers, H. stepanowi is further considered to be a complex of cryptic species predisposed to infect the same host species. While Placobdella costata is known to be the unique vector of H. stepanowi, it is only recently that independent lineages within P. costata have been illustrated—suggesting the presence of at least five unique leech species across Western Europe. The aims of our study were therefore to investigate from mitochondrial markers (COI) the genetic diversity within haemogregarines and leeches infecting freshwater turtles of the Maghreb, in order to identify processes of parasite speciation. We showed that H. stepanowi consists of at least five cryptic species in the Maghreb, while two Placobella species were identified in the same area. Although an Eastern–Western speciation pattern was apparent for both leeches and haemogregarines, we cannot make definitive conclusions regarding co-speciation patterns between parasites and vectors. However, we cannot reject the hypothesis of a very strict host–parasite specificity within leeches. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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13 pages, 2960 KiB

Open AccessArticle

Molecular Detection and Phylogenetic Analyses of Babesia spp. and Theileria spp. in Livestock in Bangladesh

by Uday Kumar Mohanta, Boniface Chikufenji, Eloiza May Galon, Shengwei Ji, Zhuowei Ma, Shimaa Abd El-Salam El-Sayed, Aaron Edmond Ringo, Thanh Thom Do and Xuenan Xuan

Microorganisms 2023, 11(6), 1563; https://doi.org/10.3390/microorganisms11061563 - 13 Jun 2023

Cited by 3 | Viewed by 2218

Abstract

Piroplasmosis, caused by Babesia spp. and Theileria spp., poses significant constraints for livestock production and upgradation in Bangladesh. Besides examining blood smears, few molecular reports are available from some selected areas in the country. Therefore, the actual scenario of piroplasmosis in Bangladesh is deficient. This study aimed to screen the piroplasms in different livestock species by molecular tools. A total of 276 blood samples were collected from cattle (Bos indicus), gayals (Bos frontalis) and goats (Capra hircus) in five geographies of Bangladesh. After that, screening was conducted through a polymerase chain reaction, and species were confirmed by sequencing. The prevalence of Babesia bigemina, B. bovis, B. naoakii, B. ovis, Theileria annulata and T. orientalis was 49.28%, 0.72%, 1.09%, 32.26%, 6.52% and 46.01%, respectively. The highest prevalence (79/109; 72.48%) of co-infections was observed with B. bigemina and T. orientalis. The phylogenetic analyses revealed that the sequences of B. bigemina (BbigRAP-1a), B. bovis (BboSBP-4), B. naoakii (AMA-1), B. ovis (ssu rRNA) and T. annulata (Tams-1) were included in one clade in the respective phylograms. In contrast, T. orientalis (MPSP) sequences were separated into two clades, corresponding to Types 5 and 7. To our knowledge, this is the first molecular report on piroplasms in gayals and goats in Bangladesh. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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16 pages, 5445 KiB

Open AccessArticle

TgKDAC4: A Unique Deacetylase of Toxoplasma’s Apicoplast

by Mariana Sayuri Ishikawa Fragoso, Caroline Moraes de Siqueira, Francisca Nathália Luna Vitorino, Alexandre Zanatta Vieira, Érica Santos Martins-Duarte, Helisson Faoro, Júlia Pinheiro Chagas da Cunha, Andréa Rodrigues Ávila and Sheila Cristina Nardelli

Microorganisms 2023, 11(6), 1558; https://doi.org/10.3390/microorganisms11061558 - 12 Jun 2023

Cited by 2 | Viewed by 1334

Abstract

Toxoplasma gondii is an obligate intracellular parasite of the phylum Apicomplexa and causes toxoplasmosis infections, a disease that affects a quarter of the world’s population and has no effective cure. Epigenetic regulation is one of the mechanisms controlling gene expression and plays an essential role in all organisms. Lysine deacetylases (KDACs) act as epigenetic regulators affecting gene silencing in many eukaryotes. Here, we focus on TgKDAC4, an enzyme unique to apicomplexan parasites, and a class IV KDAC, the least-studied class of deacetylases so far. This enzyme shares only a portion of the specific KDAC domain with other organisms. Phylogenetic analysis from the TgKDAC4 domain shows a putative prokaryotic origin. Surprisingly, TgKDAC4 is located in the apicoplast, making it the only KDAC found in this organelle to date. Transmission electron microscopy assays confirmed the presence of TgKDAC4 in the periphery of the apicoplast. We identified possible targets or/and partners of TgKDAC4 by immunoprecipitation assays followed by mass spectrometry analysis, including TgCPN60 and TgGAPDH2, both located at the apicoplast and containing acetylation sites. Understanding how the protein works could provide new insights into the metabolism of the apicoplast, an essential organelle for parasite survival. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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11 pages, 1927 KiB

Open AccessCommunication

Molecular Screening of Haemogregarine Hemoparasites (Apicomplexa: Adeleorina: Haemogregarinidae) in Populations of Native and Introduced Pond Turtles in Eastern Europe

by Marko Maričić, Gorana Danon, J. Filipe Faria and D. James Harris

Microorganisms 2023, 11(4), 1063; https://doi.org/10.3390/microorganisms11041063 - 19 Apr 2023

Cited by 3 | Viewed by 1363

Abstract

Haemogregarines (Apicomplexa: Adeleorina) are the most common and widespread reptilian blood parasites. Haemogregarina stepanowi was the first haemogregarine described from a reptile, the European pond turtle Emys orbicularis, and initial assessments indicated it was widespread across different pond turtle host species across much of Europe, the Middle East and North Africa. However, recent molecular assessments have indicated the presence of multiple genetically distinct forms in North Africa and the Iberian Peninsula, and extensive mixed infections which may be associated with a negative impact on the hosts. Here, we screened two native species, E. orbicularis and Mauremys rivulata, and the introduced Trachemys scripta from Serbia and North Macedonia for haemogregarines by amplifying and sequencing part of the 18S rRNA gene of these parasites, and used a standard DNA barcoding approach to identify leeches, the final host, attached to pond turtles. Our results again demonstrate the occurrence of considerable diversity of parasites in the analysed pond turtle species, and that T. scripta are likely infected by local haemogregarine parasites, and not those that are found in its native range. Leeches were identified as Placobdella costata, part of a lineage from Northern Europe. Mixed infections within pond turtles were again common. Current haemogregarine taxonomy does not reflect the genetic diversity identified, and a full taxonomic reassessment is needed. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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Review

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16 pages, 1106 KiB

Open AccessReview

p25alpha Domain-Containing Proteins of Apicomplexans and Related Taxa

by Ferenc Orosz

Microorganisms 2023, 11(6), 1528; https://doi.org/10.3390/microorganisms11061528 - 08 Jun 2023

Cited by 2 | Viewed by 904

Abstract

TPPP (tubulin polymerization promoting protein)-like proteins contain one or more p25alpha (Pfam05517) domains. TPPP-like proteins occur in different types as determined by their length (e.g., long-, short-, truncated-, and fungal-type TPPP) and include the protein apicortin, which possesses another domain, doublecortin (DCX, Pfam 03607). These various TPPP-like proteins are found in various phylogenomic groups. In particular, short-type TPPPs and apicortin are well-represented in the Myzozoa, which include apicomplexans and related taxa, chrompodellids, dinoflagellates, and perkinsids. The long-, truncated-, and fungal-type TPPPs are not found in the myzozoans. Apicortins are found in all apicomplexans except one piroplasmid species, present in several other myzozoans, and seem to be correlated with the conoid and apical complex. Short-type TPPPs are predominantly found in myzozoans that have flagella, suggesting a role in flagellum assembly or structure. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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43 pages, 6901 KiB

Open AccessReview

Insights into the Biology of Leucocytozoon Species (Haemosporida, Leucocytozoidae): Why Is There Slow Research Progress on Agents of Leucocytozoonosis?

by Gediminas Valkiūnas and Tatjana A. Iezhova

Microorganisms 2023, 11(5), 1251; https://doi.org/10.3390/microorganisms11051251 - 09 May 2023

Cited by 8 | Viewed by 5296

Abstract

Blood parasites of the genus Leucocytozoon (Leucocytozoidae) only inhabit birds and represent a readily distinct evolutionary branch of the haemosporidians (Haemosporida, Apicomplexa). Some species cause pathology and even severe leucocytozoonosis in avian hosts, including poultry. The diversity of Leucocytozoon pathogens is remarkable, with over 1400 genetic lineages detected, most of which, however, have not been identified to the species level. At most, approximately 45 morphologically distinct species of Leucocytozoon have been described, but only a few have associated molecular data. This is unfortunate because basic information about named and morphologically recognized Leucocytozoon species is essential for a better understanding of phylogenetically closely related leucocytozoids that are known only by DNA sequence. Despite much research on haemosporidian parasites during the past 30 years, there has not been much progress in taxonomy, vectors, patterns of transmission, pathogenicity, and other aspects of the biology of these cosmopolitan bird pathogens. This study reviewed the available basic information on avian Leucocytozoon species, with particular attention to some obstacles that prevent progress to better understanding the biology of leucocytozoids. Major gaps in current Leucocytozoon species research are discussed, and possible approaches are suggested to resolve some issues that have limited practical parasitological studies of these pathogens. Full article

(This article belongs to the Special Issue The Current View on Apicomplexan Parasites: Structure, Function, Evolution)

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