Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy
Posted on: 13 June 2023 , updated on: 3 July 2023
Preprint posted on 15 May 2023
Divide et Impera. Thanks to U-ExM, cheap and high resolution imaging maps the asexual reproduction cycle of malaria parasites in red blood cells
Selected by Nadja HümpferCategories: biochemistry, cell biology, developmental biology, microbiology
Background
Malaria is a fatal disease transmitted by parasites of the species Plasmodium. Their life cycle includes replication of the organism inside red blood cells of infected vertebrates. Five species are known to infect humans, but Plasmodium falciparum accounts for the majority of severe cases in human. Plasmodium have a complex life cycle with different stages. Their sexual reproduction takes place in insect (mostly mosquito) vectors, after which parasites at the sporozoite stage are transmitted to the human host during blood meals. Inside the human host, they first infect hepatocytes (liver stages) and then erythrocytes (blood stages). At these life stages, they reproduce asexually by duplication of genetic and cellular material to produce several merozoites inside the infected host cell. Merozoites are released and the erythrocyte is destroyed in the process, which causes the infected host to feel the typical malaria symptoms such as fever and malaise. The merozoites can then infect the next pool of erythrocytes. Depending on the duration of the replication cycle, the malaria symptoms can occur in turns of two to three days. A fraction of the parasites turns into gametocytes (sexual stage), which are ingested by the mosquito to enable transmission between the host and vector.
In this preprint, the authors use ultrastructure expansion microscopy (U-ExM) [1] to investigate the cellular organization of P. falciparum asexual reproduction in erythrocytes. This technique allows magnification by physically expanding the sample. Therefore, the resolution can be increased by the factor of expansion, 4.5-fold in the case of U-ExM. In addition, the U-ExM variety of ExM [2] is optimally suited for the staining of denatured proteins after expansion. This makes tightly packed structures accessible. In their work, Liffner & Cepeda Diaz et al. combine antibody-based staining for 13 different organelles and markers with a pan-staining [3] for cellular context. The pan-protein staining was achieved by labelling the entire protein content with NHS-ester coupled dyes. They also visualized the membranes by employing BODIPY TRc. The EM-like context together with specific information from antibodies allowed the authors to collect a full ‘atlas’ of P. falciparum development in erythrocytes.
Key findings
Overall, the study provides a comprehensive overview of the P. falciparum developmental stages inside red blood cells. As the authors frame it, they put together an ‘atlas’ of unprecedented detail that shows how the parasite transforms from the ‘ring state’, right after the infection, into a trophozoite and finally into the schizont to produce the merozoites that are the infectious particles. The improved resolution of U-ExM, together with the decrowding effect and the cellular context, allows the authors to describe the Plasmodium life cycle in great detail and to support common hypotheses in the field with their data.
The emphasis of the study is the biological side; the method was merely altered compared to the original U-ExM protocol. In this respect, the preprint is of particular interest to Plasmodium biologists, who are at ease with the specific Plasmodium terminology of organelles and developmental stages. For an overview of the intraerythrocytic cycle of P. falciparum, check out this schematic as published in [4].
Glossary
Apicoplast | A plastid found in most Apicomplexa. It is non-photosynthetic but indispensable for the invasion of host cells. |
Basal Complex | A ring-shaped protein complex that segments the multinucleated schizont into individual merozoites during cytokinesis. |
Cytostome | Endocytic compartment that allows the parasite to feed of the host red blood cell’s hemoglobin. |
Merozoite | Infectious unit of Plasmodium that is produced after the segmentation of the schizont into multiple of merozoites. |
Rhoptry | Secretory organelle inside the merozoites. It secretes proteins that are involved in host cell invasion |
Ring | The first stage after Plasmodium infects the red blood cell. |
Schizogony | The process of multiple rounds of mitosis and nuclear fission, followed by cytokinesis; which allows the Plasmodium to replicate asexually. |
Schizont | Multinucleated stage of Plasmodium inside the red blood cell. |
Trophozoite | Feeding stage of Plasmodium inside the red blood cell. |
The MTOC has an important part in scaffolding organelles during segmentation
A big section of the study focuses on the role of the microtubule organizing center (MTOC) in mitosis and cytokinesis. The MTOC could be visualized by NHS-ester staining. Imaging suggested that the MTOC anchors the mitotic nuclei to the plasma membrane in the trophozoite. The MTOC cytoplasmic extensions remained in contact with different organelles during cytokinesis, such as the Golgi, the rhoptries, and the basal complex. The MTOC also associated with the mitochondrion and the apicoplast at the end of segmentation, anchoring them to a common point inside the cell. Therefore, the authors assign the MTOC the important role of controlling the apico-basal polarity during schizogony.
Organelle segmentation follows the branching point fission model
An interesting section of the study investigates the fission of two organelles: the mitochondrion and the apicoplast. An early trophozoite has one of each organelle, but during schizogony, both need to increase their size and volume and be split into smaller bits to be inherited by the developing merozoites upon segmentation. Staining of mitochondrion and apicoplast markers, together with the basal complex that is responsible for the segmentation of the schizont into smaller individual units (i.e. the merozoites), argues for a branching point fission model: That is, first, the organelles grow; second, they are segmented at a few points. Finally, they undergo another round of fission to produce the accurate number of organelles mirroring the number of merozoites.
NHS-ester staining provides contrast to depict the cytostome of P. falciparum
The pan-protein staining with NHS-ester coupled dyes highlights several protein-dense structures in the Plasmodium cell. Some of them are clearly identifiable by their morphology (such as the rhoptry bulbs, which are discussed below). The authors noticed a small ring-like structure at the interface of the parasite membrane and the parasitophorous vacuole that harbors Plasmodium inside the erythrocyte. They speculated this to reflect the collar of the cytostome, an endocytic structure that allows the parasite to feed on hemoglobin from the erythrocyte cytoplasm. They used Kelch13 (K13), a recently described marker for the endocytic micropore in Toxoplasma (Plasmodium and Toxoplasma are both members of the phylum Apicomplexa of parasites) to detect the collar in Plasmodium. K13 localized to the protein-dense rings and was confirmed as a marker for the cytostome. Altering the fixation protocol even allowed the authors to visualize the content of the endocytic pore.
Asymmetric rhoptry biogenesis
Rhoptries are organelles that merozoites need to invade erythrocytes. Like other organelles, they need to be multiplied and segregated equally between the developing merozoites. The authors observed two interesting aspects of rhoptry biogenesis. First, they noticed a tight association between the rhoptries and the microtubule organizing center (MTOC) throughout schizogony. Second, they observed different densities in terms of protein content in the rhoptries. Surprisingly, the differences in protein density did not reflect the maturity of the rhoptry. At least the localization of a specific marker of mature rhoptries, RON4, to the less dense rhoptries suggested that density is not positively correlated with rhoptry age.
What I like about this preprint
This work shows the application of an upcoming imaging technology. Expansion microscopy circumvents the diffraction limit of fluorescent microcopy by physical expansion of the sample. Since its first publication in 2015 [2], many methodological papers have been published, focusing on the improvement of the expansion factor or the combination of expansion microscopy with other super-resolution imaging techniques. As is often the case with the advent of a new technique, it takes time until the method can be used to answer biological questions. In their study, Liffner & Cepeda Diaz et al. prove the value of ExM to biology and generate an impressive amount of data, which will be made available to the community so people can browse the atlas and answer additional questions. They achieved this by taking advantage of the traits of U-ExM. It is cost effective, easy to implement with already established staining protocols, increases the spatial resolution and provides ultrastructural context. Therefore, it could serve as a bridging technology between super-resolution fluorescence imaging and electron microscopy.
I especially like how biologists working with diverse model systems adopt ExM. They apply the general protocol to different organisms, such as Plasmodia [5], Chlamydia [6], Trypanosoma [7] and Toxoplasma [8]. ExM was even explored on the pilot expedition of EMBL’s Traversing European Coastlines project to study plankton.
The authors also point out structures that could not be resolved with their protocol. They find that the hemozoin crystal that fills the inside of the schizont could not be detected. This is likely due to its composition. Hemozoin is produced by the parasite during digestion of hemoglobin. It leaves the heme groups and turns them into a crystalline form, which likely cannot be expanded. The different layers of parasite and cellular membranes were too dense to be distinguished with the improved resolution, unfortunately.
Nevertheless, this Plasmodium atlas could become a powerful resource for researchers in the field, especially once the imaging data will be publicly available.
The preprint is published in eLife together with reviewers’ comments.
References
[2] Chen, F., et al. (2015). “Optical imaging. Expansion microscopy.” Science 347(6221): 543-548.
doi: https://doi.org/10.1242/prelights.34838
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