Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle

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

Deadline for manuscript submissions: closed (30 April 2022) | Viewed by 30093

Special Issue Editors

Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic
Interests: parasitic protists; Apicomplexa; parasitism strategies; cell motility; host–parasite interactions; in vivo and in vitro experimental studies
Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic
Interests: leishmaniasis; sand fly saliva; host–parasite immune interactions; vector–host immune interactions
Parasites and Free-Living Protists (UMR7245 CNRS-MNHN), Department “Adaptations of living organisms”, National Museum of Natural History, Paris, France
Interests: parasitic protists; Apicomplexa; Giardia; host-parasite interactions; parasite control mechanisms; in vitro and in vivo experimental studies

Special Issue Information

Dear Colleagues,

Parasitic protists unite a wide spectrum of unicellular eukaryotic pathogens, comprising agents of significant human and animal diseases such as malaria, toxoplasmosis, amoebic meningitis, sleeping sickness, leishmaniosis, and diarrheal illness of protozoan origin (e.g. amoebiasis, cryptosporidiosis and giardiasis). While the nature of the diseases and the transmission modes (e.g. vector-borne, food-/water-borne, by contact or fomites) vary widely among parasitic protists, they generally constitute the health management challenge and have a significant impact on the global economy. Given the growing number of emerging and re-emerging diseases caused by parasitic protists, there is an urgent need to implement new strategies in vaccine development and therapeutic interventions. The causative agents of these diseases have evolved a wide range of unique adaptations to parasitism, leading to different strategies of invasion, proliferation and survival within their hosts’ appropriate niches, as well as transmission modes, which hampers our effort to control them. These allow them to manipulate the host (or its cells), to modulate or evade the host immune responses and even to use host metabolic processes for their own benefit.

To illustrate the biological diversity behind the parasitism strategies of protists, this Special Issue of Microorganisms invites researchers to present their original research findings, up-to-date reviews or short communications concerning any aspect related to the subject, including, but not limited to, evolutionary trends in successful parasitism, invasion and survival strategies, host-parasite interactions (immune, cellular, metabolic, etc.), virulence mechanisms, and pathogenesis. The main goal is to provide a platform to exchange a current knowledge and to demonstrate that parasitism strategies of these organisms are so specific and unique that they need to be addressed individually in search for modern prophylactic strategies, diagnostic and therapeutic tools.

Dr. Andrea Bardůnek Valigurová
Dr. Iva Kolářová
Prof. Dr. Isabelle Florent
Guest Editors

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Keywords

  • Evolutionary adaptations
  • Invasion strategies
  • Host–parasite interactions
  • Host cell remodeling
  • Parasite escape strategies
  • Immune modulation
  • Cell biology

Published Papers (11 papers)

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Editorial

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3 pages, 207 KiB  
Editorial
Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle
by Iva Kolářová, Isabelle Florent and Andrea Valigurová
Microorganisms 2022, 10(8), 1560; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10081560 - 03 Aug 2022
Cited by 1 | Viewed by 1566
Abstract
Parasitic protists cause some of the most well-known human and animal diseases such as malaria, toxoplasmosis, amoebic meningitis, sleeping sickness, leishmaniosis, and diarrheal illness of protozoan origin (e [...] Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)

Research

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10 pages, 1507 KiB  
Article
Genetic Diversity and Phylogenetic Relatedness of Plasmodium ovale curtisi and Plasmodium ovale wallikeri in sub-Saharan Africa
by Mary A. Oboh and Bolaji N. Thomas
Microorganisms 2022, 10(6), 1147; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10061147 - 02 Jun 2022
Cited by 1 | Viewed by 1614
Abstract
P. ovale was until recently thought to be a single unique species. However, the deployment of more sensitive tools has led to increased diagnostic sensitivity, including new evidence supporting the presence of two sympatric species: P. ovale curtisi (Poc) and P. ovale wallikeri [...] Read more.
P. ovale was until recently thought to be a single unique species. However, the deployment of more sensitive tools has led to increased diagnostic sensitivity, including new evidence supporting the presence of two sympatric species: P. ovale curtisi (Poc) and P. ovale wallikeri (Pow). The increased reports and evolution of P. ovale subspecies are concerning for sub-Saharan Africa where the greatest burden of malaria is borne. Employing published sequence data, we set out to decipher the genetic diversity and phylogenetic relatedness of P. ovale curtisi and P. ovale wallikeri using the tryptophan-rich protein and small subunit ribosomal RNA genes from Gabon, Senegal, Ethiopia and Kenya. Higher number of segregating sites were recorded in Poc isolates from Gabon than from Ethiopia, with a similar trend in the number of haplotypes. With regards to Pow, the number of segregating sites and haplotypes from Ethiopia were higher than from those in Gabon. Poc from Kenya, had higher segregating sites (20), and haplotypes (4) than isolates from Senegal (8 and 3 respectively), while nucleotide from Senegal were more diverse (θw = 0.02159; π = 0.02159) than those from Kenya (θw = 0.01452; π = 0.01583). Phylogenetic tree construction reveal two large clades with Poc from Gabon and Ethiopia, and distinct Gabonese and Ethiopian clades on opposite ends. A similar observation was recorded for the phylogeny of Poc isolates from Kenya and Senegal. With such results, there is a high potential that ovale malaria control measures deployed in one country may be effective in the other since parasite from both countries show some degree of relatedness. How this translates to malaria control efforts throughout the continent would be next step deserving more studies. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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23 pages, 5780 KiB  
Article
Neofunctionalization of Glycolytic Enzymes: An Evolutionary Route to Plant Parasitism in the Oomycete Phytophthora nicotianae
by Marie-Line Kuhn, Jo-Yanne Le Berre, Naima Kebdani-Minet and Franck Panabières
Microorganisms 2022, 10(2), 281; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10020281 - 25 Jan 2022
Cited by 3 | Viewed by 2623
Abstract
Oomycetes, of the genus Phytophthora, comprise of some of the most devastating plant pathogens. Parasitism of Phytophthora results from evolution from an autotrophic ancestor and adaptation to a wide range of environments, involving metabolic adaptation. Sequence mining showed that Phytophthora spp. display [...] Read more.
Oomycetes, of the genus Phytophthora, comprise of some of the most devastating plant pathogens. Parasitism of Phytophthora results from evolution from an autotrophic ancestor and adaptation to a wide range of environments, involving metabolic adaptation. Sequence mining showed that Phytophthora spp. display an unusual repertoire of glycolytic enzymes, made of multigene families and enzyme replacements. To investigate the impact of these gene duplications on the biology of Phytophthora and, eventually, identify novel functions associated to gene expansion, we focused our study on the first glycolytic step on P. nicotianae, a broad host range pathogen. We reveal that this step is committed by a set of three glucokinase types that differ by their structure, enzymatic properties, and evolutionary histories. In addition, they are expressed differentially during the P. nicotianae life cycle, including plant infection. Last, we show that there is a strong association between the expression of a glucokinase member in planta and extent of plant infection. Together, these results suggest that metabolic adaptation is a component of the processes underlying evolution of parasitism in Phytophthora, which may possibly involve the neofunctionalization of metabolic enzymes. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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11 pages, 1465 KiB  
Article
Complete Life Cycle of Trypanosoma thomasbancrofti, an Avian Trypanosome Transmitted by Culicine Mosquitoes
by Magdaléna Fialová, Anežka Santolíková, Anna Brotánková, Jana Brzoňová and Milena Svobodová
Microorganisms 2021, 9(10), 2101; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9102101 - 05 Oct 2021
Cited by 7 | Viewed by 1648
Abstract
Avian trypanosomes are cosmopolitan and common protozoan parasites of birds; nevertheless, knowledge of their life cycles and vectors remains incomplete. Mosquitoes have been confirmed as vectors of Trypanosoma culicavium and suggested as vectors of T. thomasbancrofti; however, transmission has been experimentally confirmed [...] Read more.
Avian trypanosomes are cosmopolitan and common protozoan parasites of birds; nevertheless, knowledge of their life cycles and vectors remains incomplete. Mosquitoes have been confirmed as vectors of Trypanosoma culicavium and suggested as vectors of T. thomasbancrofti; however, transmission has been experimentally confirmed only for the former species. This study aims to confirm the experimental transmission of T. thomasbancrofti to birds and its localization in vectors. Culex pipiens were fed on blood using four strains of T. thomasbancrofti, isolated from vectors and avian hosts; all strains established infections, and three of them were able to develop high infection rates in mosquitoes. The infection rate of the culicine isolates was 5–28% for CUL15 and 48–81% for CUL98, 67–92% for isolate OF19 from hippoboscid fly, while the avian isolate PAS343 ranged between 48% and 92%, and heavy infections were detected in 90% of positive females. Contrary to T. culicavium, trypanosomes were localized in the hindgut, where they formed rosettes with the occurrence of free epimastigotes in the hindgut and midgut during late infections. Parasites occurred in urine droplets produced during mosquito prediuresis. Transmission to birds was achieved by the ingestion of mosquito guts containing trypanosomes and via the conjunctiva. Bird infection was proven by blood cultivation and xenodiagnosis; mature infections were present in the dissected guts of 24–26% of mosquitoes fed on infected birds. The prevalence of T. thomasbancrofti in vectors in nature and in avian populations is discussed in this paper. This study confirms the vectorial capacity of culicine mosquitoes for T. thomasbancrofti, a trypanosome related to T. avium, and suggests that prediuresis might be an effective mode of trypanosome transmission. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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15 pages, 6583 KiB  
Article
Infection of Slugs with Theronts of the Ciliate Protozoan, Tetrahymena rostrata
by Ruth E. Haites, Anne E. Watt, Derek A. Russell and Helen Billman-Jacobe
Microorganisms 2021, 9(9), 1970; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9091970 - 16 Sep 2021
Cited by 4 | Viewed by 2089
Abstract
Tetrahymena rostrata is a free-living ciliated protozoan and is a facultative parasite of some species of terrestrial mollusks. It is a potential biopesticide of pest slugs, such as the grey field slug, which cause considerable damage to crops. T. rostrata has several developmental [...] Read more.
Tetrahymena rostrata is a free-living ciliated protozoan and is a facultative parasite of some species of terrestrial mollusks. It is a potential biopesticide of pest slugs, such as the grey field slug, which cause considerable damage to crops. T. rostrata has several developmental forms. Homogeneous preparations of the feeding stage cells (trophonts) and excysted stage cells (theronts) were compared for their ability to infect and kill Deroceras reticulatum slugs. Theronts were more effective and remained viable and infective, even after prolonged starvation. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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17 pages, 3673 KiB  
Article
Glucose-6-Phosphate Dehydrogenase::6-Phosphogluconolactonase from the Parasite Giardia lamblia. A Molecular and Biochemical Perspective of a Fused Enzyme
by Laura Morales-Luna, Abigail González-Valdez, Beatriz Hernández-Ochoa, Roberto Arreguin-Espinosa, Daniel Ortega-Cuellar, Rosa Angélica Castillo-Rodríguez, Víctor Martínez-Rosas, Noemi Cárdenas-Rodríguez, Sergio Enríquez-Flores, Luis Miguel Canseco-Ávila, Verónica Pérez de la Cruz, Fernando Gómez-Chávez and Saúl Gómez-Manzo
Microorganisms 2021, 9(8), 1678; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9081678 - 07 Aug 2021
Cited by 5 | Viewed by 2288
Abstract
Giardia lamblia is a single-celled eukaryotic parasite with a small genome and is considered an early divergent eukaryote. The pentose phosphate pathway (PPP) plays an essential role in the oxidative stress defense of the parasite and the production of ribose-5-phosphate. In this parasite, [...] Read more.
Giardia lamblia is a single-celled eukaryotic parasite with a small genome and is considered an early divergent eukaryote. The pentose phosphate pathway (PPP) plays an essential role in the oxidative stress defense of the parasite and the production of ribose-5-phosphate. In this parasite, the glucose-6-phosphate dehydrogenase (G6PD) is fused with the 6-phosphogluconolactonase (6PGL) enzyme, generating the enzyme named G6PD::6PGL that catalyzes the first two steps of the PPP. Here, we report that the G6PD::6PGL is a bifunctional enzyme with two catalytically active sites. We performed the kinetic characterization of both domains in the fused G6PD::6PGL enzyme, as well as the individual cloned G6PD. The results suggest that the catalytic activity of G6PD and 6PGL domains in the G6PD::6PGL enzyme are more efficient than the individual proteins. Additionally, using enzymatic and mass spectrometry assays, we found that the final metabolites of the catalytic reaction of the G6PD::6PGL are 6-phosphoglucono-δ-lactone and 6-phosphogluconate. Finally, we propose the reaction mechanism in which the G6PD domain performs the catalysis, releasing 6-phosphoglucono-δ-lactone to the reaction medium. Then, this metabolite binds to the 6PGL domain catalyzing the hydrolysis reaction and generating 6-phosphogluconate. The structural difference between the G. lamblia fused enzyme G6PD::6PGL with the human G6PD indicate that the G6PD::6PGL is a potential drug target for the rational synthesis of novels anti-Giardia drugs. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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14 pages, 3158 KiB  
Article
Genome-Wide Expression Patterns of Rhoptry Kinases during the Eimeria tenella Life-Cycle
by Adeline Ribeiro E Silva, Alix Sausset, Françoise I. Bussière, Fabrice Laurent, Sonia Lacroix-Lamandé and Anne Silvestre
Microorganisms 2021, 9(8), 1621; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9081621 - 29 Jul 2021
Cited by 8 | Viewed by 2071
Abstract
Kinome from apicomplexan parasites is composed of eukaryotic protein kinases and Apicomplexa specific kinases, such as rhoptry kinases (ROPK). Ropk is a gene family that is known to play important roles in host–pathogen interaction in Toxoplasma gondii but is still poorly described in [...] Read more.
Kinome from apicomplexan parasites is composed of eukaryotic protein kinases and Apicomplexa specific kinases, such as rhoptry kinases (ROPK). Ropk is a gene family that is known to play important roles in host–pathogen interaction in Toxoplasma gondii but is still poorly described in Eimeria tenella, the parasite responsible for avian coccidiosis worldwide. In the E. tenella genome, 28 ropk genes are predicted and could be classified as active (n = 7), inactive (incomplete catalytic triad, n = 12), and non-canonical kinases (active kinase with a modified catalytic triad, n = 9). We characterized the ropk gene expression patterns by real-time quantitative RT-PCR, normalized by parasite housekeeping genes, during the E. tenella life-cycle. Analyzed stages were: non-sporulated oocysts, sporulated oocysts, extracellular and intracellular sporozoites, immature and mature schizonts I, first- and second-generation merozoites, and gametes. Transcription of all those predicted ropk was confirmed. The mean intensity of transcription was higher in extracellular stages and 7–9 ropk were specifically transcribed in merozoites in comparison with sporozoites. Transcriptional profiles of intracellular stages were closely related to each other, suggesting a probable common role of ROPKs in hijacking signaling pathways and immune responses in infected cells. These results provide a solid basis for future functional analysis of ROPK from E. tenella. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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14 pages, 3622 KiB  
Article
A Single-Pass Type I Membrane Protein from the Apicomplexan Parasite Cryptosporidium parvum with Nanomolar Binding Affinity to Host Cell Surface
by Tianyu Zhang, Xin Gao, Dongqiang Wang, Jixue Zhao, Nan Zhang, Qiushi Li, Guan Zhu and Jigang Yin
Microorganisms 2021, 9(5), 1015; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9051015 - 08 May 2021
Cited by 7 | Viewed by 2385
Abstract
Cryptosporidium parvum is a globally recognized zoonotic parasite of medical and veterinary importance. This parasite mainly infects intestinal epithelial cells and causes mild to severe watery diarrhea that could be deadly in patients with weakened or defect immunity. However, its molecular interactions with [...] Read more.
Cryptosporidium parvum is a globally recognized zoonotic parasite of medical and veterinary importance. This parasite mainly infects intestinal epithelial cells and causes mild to severe watery diarrhea that could be deadly in patients with weakened or defect immunity. However, its molecular interactions with hosts and pathogenesis, an important part in adaptation of parasitic lifestyle, remain poorly understood. Here we report the identification and characterization of a C. parvum T-cell immunomodulatory protein homolog (CpTIPH). CpTIPH is a 901-aa single-pass type I membrane protein encoded by cgd5_830 gene that also contains a short Vibrio, Colwellia, Bradyrhizobium and Shewanella (VCBS) repeat and relatively long integrin alpha (ITGA) N-terminus domain. Immunofluorescence assay confirmed the location of CpTIPH on the cell surface of C. parvum sporozoites. In congruence with the presence of VCBS repeat and ITGA domain, CpTIPH displayed high, nanomolar binding affinity to host cell surface (i.e., Kd(App) at 16.2 to 44.7 nM on fixed HCT-8 and CHO-K1 cells, respectively). The involvement of CpTIPH in the parasite invasion is partly supported by experiments showing that an anti-CpTIPH antibody could partially block the invasion of C. parvum sporozoites into host cells. These observations provide a strong basis for further investigation of the roles of CpTIPH in parasite-host cell interactions. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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24 pages, 6357 KiB  
Article
Cryptosporidium myocastoris n. sp. (Apicomplexa: Cryptosporidiidae), the Species Adapted to the Nutria (Myocastor coypus)
by Jana Ježková, Zlata Limpouchová, Jitka Prediger, Nikola Holubová, Bohumil Sak, Roman Konečný, Dana Květoňová, Lenka Hlásková, Michael Rost, John McEvoy, Dušan Rajský, Yaoyu Feng and Martin Kváč
Microorganisms 2021, 9(4), 813; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9040813 - 12 Apr 2021
Cited by 33 | Viewed by 2980
Abstract
Cryptosporidium spp., common parasites of vertebrates, remain poorly studied in wildlife. This study describes the novel Cryptosporidium species adapted to nutrias (Myocastor coypus). A total of 150 faecal samples of feral nutria were collected from locations in the Czech Republic and [...] Read more.
Cryptosporidium spp., common parasites of vertebrates, remain poorly studied in wildlife. This study describes the novel Cryptosporidium species adapted to nutrias (Myocastor coypus). A total of 150 faecal samples of feral nutria were collected from locations in the Czech Republic and Slovakia and examined for Cryptosporidium spp. oocysts and specific DNA at the SSU, actin, HSP70, and gp60 loci. Molecular analyses revealed the presence of C. parvum (n = 1), C. ubiquitum subtype family XIId (n = 5) and Cryptosporidium myocastoris n. sp. XXIIa (n = 2), and XXIIb (n = 3). Only nutrias positive for C. myocastoris shed microscopically detectable oocysts, which measured 4.8–5.2 × 4.7–5.0 µm, and oocysts were infectious for experimentally infected nutrias with a prepatent period of 5–6 days, although not for mice, gerbils, or chickens. The infection was localised in jejunum and ileum without observable macroscopic changes. The microvilli adjacent to attached stages responded by elongating. Clinical signs were not observed in naturally or experimentally infected nutrias. Phylogenetic analyses at SSU, actin, and HSP70 loci demonstrated that C. myocastoris n. sp. is distinct from other valid Cryptosporidium species. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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Review

Jump to: Editorial, Research

22 pages, 3098 KiB  
Review
Hide-and-Seek: A Game Played between Parasitic Protists and Their Hosts
by Iva Kolářová and Andrea Valigurová
Microorganisms 2021, 9(12), 2434; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9122434 - 25 Nov 2021
Cited by 9 | Viewed by 3049
Abstract
After invading the host organism, a battle occurs between the parasitic protists and the host’s immune system, the result of which determines not only whether and how well the host survives and recovers, but also the fate of the parasite itself. The exact [...] Read more.
After invading the host organism, a battle occurs between the parasitic protists and the host’s immune system, the result of which determines not only whether and how well the host survives and recovers, but also the fate of the parasite itself. The exact weaponry of this battle depends, among others, on the parasite localisation. While some parasitic protists do not invade the host cell at all (extracellular parasites), others have developed successful intracellular lifestyles (intracellular parasites) or attack only the surface of the host cell (epicellular parasites). Epicellular and intracellular protist parasites have developed various mechanisms to hijack host cell functions to escape cellular defences and immune responses, and, finally, to gain access to host nutrients. They use various evasion tactics to secure the tight contact with the host cell and the direct nutrient supply. This review focuses on the adaptations and evasion strategies of parasitic protists on the example of two very successful parasites of medical significance, Cryptosporidium and Leishmania, while discussing different localisation (epicellular vs. intracellular) with respect to the host cell. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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31 pages, 9758 KiB  
Review
Nutrient Acquisition and Attachment Strategies in Basal Lineages: A Tough Nut to Crack in the Evolutionary Puzzle of Apicomplexa
by Andrea Valigurová and Isabelle Florent
Microorganisms 2021, 9(7), 1430; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9071430 - 02 Jul 2021
Cited by 11 | Viewed by 3342
Abstract
Apicomplexa are unicellular eukaryotes that parasitise a wide spectrum of invertebrates and vertebrates, including humans. In their hosts, they occupy a variety of niches, from extracellular cavities (intestine, coelom) to epicellular and intracellular locations, depending on the species and/or developmental stages. During their [...] Read more.
Apicomplexa are unicellular eukaryotes that parasitise a wide spectrum of invertebrates and vertebrates, including humans. In their hosts, they occupy a variety of niches, from extracellular cavities (intestine, coelom) to epicellular and intracellular locations, depending on the species and/or developmental stages. During their evolution, Apicomplexa thus developed an exceptionally wide range of unique features to reach these diversified parasitic niches and to survive there, at least long enough to ensure their own transmission or that of their progeny. This review summarises the current state of knowledge on the attachment/invasive and nutrient uptake strategies displayed by apicomplexan parasites, focusing on trophozoite stages of their so far poorly studied basal representatives, which mostly parasitise invertebrate hosts. We describe their most important morphofunctional features, and where applicable, discuss existing major similarities and/or differences in the corresponding mechanisms, incomparably better described at the molecular level in the more advanced Apicomplexa species, of medical and veterinary significance, which mainly occupy intracellular niches in vertebrate hosts. Full article
(This article belongs to the Special Issue Parasitic Protists: Diversity of Adaptations to a Parasitic Lifestyle)
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