Most cited article - PubMed ID 31422883
Multiple Independent Origins of Apicomplexan-Like Parasites
Understanding the origin of eukaryotic cells is one of the most difficult problems in all of biology. A key challenge relevant to the question of eukaryogenesis is reconstructing the gene repertoire of the last eukaryotic common ancestor (LECA). As data sets grow, sketching an accurate genomics-informed picture of early eukaryotic cellular complexity requires provision of analytical resources and a commitment to data sharing. Here, we summarise progress towards understanding the biology of LECA and outline a community approach to inferring its wider gene repertoire. Once assembled, a robust LECA gene set will be a useful tool for evaluating alternative hypotheses about the origin of eukaryotes and understanding the evolution of traits in all descendant lineages, with relevance in diverse fields such as cell biology, microbial ecology, biotechnology, agriculture, and medicine. In this Consensus View, we put forth the status quo and an agreed path forward to reconstruct LECA's gene content.
Complete plastid loss seems to be very rare among secondarily non-photosynthetic eukaryotes. Leukarachnion sp. PRA-24, an amoeboid colourless protist related to the photosynthetic algal class Synchromophyceae (Ochrophyta), is a candidate for such a case based on a previous investigation by transmission electron microscopy. Here, we characterize this organism in further detail and describe it as Leucomyxa plasmidifera gen. et sp. nov., additionally demonstrating it is the first known representative of a broader clade of non-photosynthetic ochrophytes. We recovered its complete plastid genome, exhibiting a reduced gene set similar to plastomes of other non-photosynthetic ochrophytes, yet being even more extreme in sequence divergence. Identification of components of the plastid protein import machinery in the L. plasmidifera transcriptome assembly corroborated that the organism possesses a cryptic plastid organelle. According to our bioinformatic reconstruction, the plastid contains a unique combination of biosynthetic pathways producing haem, a folate precursor and tocotrienols. As another twist to its organellar biology, L. plasmidifera turned out to contain an unusual long insertion in its mitogenome related to a newly discovered mitochondrial plasmid exhibiting unprecedented features in terms of its size and coding capacity. Combined, our work uncovered further striking outcomes of the evolutionary course of semiautonomous organelles in protists.
- Keywords
- Leukarachnion, mitochondrial plasmids, non-photosynthetic plastid, plastid evolution, plastid genome, stramenopiles,
- MeSH
- Phylogeny * MeSH
- Genome, Mitochondrial MeSH
- Genome, Plastid * MeSH
- Mitochondria genetics metabolism MeSH
- Evolution, Molecular MeSH
- Plastids * genetics metabolism MeSH
- Plasmids * genetics MeSH
- Publication type
- Journal Article MeSH
DNA polymerases synthesize DNA from deoxyribonucleotides in a semiconservative manner and serve as the core of DNA replication and repair machinery. In eukaryotic cells, there are 2 genome-containing organelles, mitochondria, and plastids, which were derived from an alphaproteobacterium and a cyanobacterium, respectively. Except for rare cases of genome-lacking mitochondria and plastids, both organelles must be served by nucleus-encoded DNA polymerases that localize and work in them to maintain their genomes. The evolution of organellar DNA polymerases has yet to be fully understood because of 2 unsettled issues. First, the diversity of organellar DNA polymerases has not been elucidated in the full spectrum of eukaryotes. Second, it is unclear when the DNA polymerases that were used originally in the endosymbiotic bacteria giving rise to mitochondria and plastids were discarded, as the organellar DNA polymerases known to date show no phylogenetic affinity to those of the extant alphaproteobacteria or cyanobacteria. In this study, we identified from diverse eukaryotes 134 family A DNA polymerase sequences, which were classified into 10 novel types, and explored their evolutionary origins. The subcellular localizations of selected DNA polymerases were further examined experimentally. The results presented here suggest that the diversity of organellar DNA polymerases has been shaped by multiple transfers of the PolI gene from phylogenetically broad bacteria, and their occurrence in eukaryotes was additionally impacted by secondary plastid endosymbioses. Finally, we propose that the last eukaryotic common ancestor may have possessed 2 mitochondrial DNA polymerases, POP, and a candidate of the direct descendant of the proto-mitochondrial DNA polymerase I, rdxPolA, identified in this study.
- Keywords
- DNA polymerase, endosymbiosis, last eukaryotic common ancestor, lateral gene transfer, mitochondria, plastids,
- MeSH
- DNA-Directed DNA Polymerase genetics MeSH
- Phylogeny MeSH
- Mitochondria MeSH
- Organelles * genetics MeSH
- Plastids genetics MeSH
- Cyanobacteria * genetics MeSH
- Symbiosis MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA-Directed DNA Polymerase MeSH
Microbial eukaryotes are important components of marine ecosystems, and the Marine Alveolates (MALVs) are consistently both abundant and diverse in global environmental sequencing surveys. MALVs are dinoflagellates that are thought to be parasites of other protists and animals, but the lack of data beyond ribosomal RNA gene sequences from all but a few described species means much of their biology and evolution remain unknown. Using single-cell transcriptomes from several MALVs and their free-living relatives, we show that MALVs evolved independently from two distinct, free-living ancestors and that their parasitism evolved in parallel. Phylogenomics shows one subgroup (MALV-II and -IV, or Syndiniales) is related to a novel lineage of free-living, eukaryovorous predators, the eleftherids, while the other (MALV-I, or Ichthyodinida) is related to the free-living predator Oxyrrhis and retains proteins targeted to a non-photosynthetic plastid. Reconstructing the evolution of photosynthesis, plastids, and parasitism in early-diverging dinoflagellates shows a number of parallels with the evolution of their apicomplexan sisters. In both groups, similar forms of parasitism evolved multiple times and photosynthesis was lost many times. By contrast, complete loss of the plastid organelle is infrequent and, when this does happen, leaves no residual genes.
- MeSH
- Dinoflagellida * genetics MeSH
- Ecosystem MeSH
- Photosynthesis genetics MeSH
- Phylogeny MeSH
- Parasites * genetics MeSH
- Plastids genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Apicomplexans and related lineages comprise many obligate symbionts of animals; some of which cause notorious diseases such as malaria. They evolved from photosynthetic ancestors and transitioned into a symbiotic lifestyle several times, giving rise to species with diverse non-photosynthetic plastids. Here, we sought to reconstruct the evolution of the cryptic plastids in the apicomplexans, chrompodellids, and squirmids (ACS clade) by generating five new single-cell transcriptomes from understudied gregarine lineages, constructing a robust phylogenomic tree incorporating all ACS clade sequencing datasets available, and using these to examine in detail, the evolutionary distribution of all 162 proteins recently shown to be in the apicoplast by spatial proteomics in Toxoplasma. This expanded homology-based reconstruction of plastid proteins found in the ACS clade confirms earlier work showing convergence in the overall metabolic pathways retained once photosynthesis is lost, but also reveals differences in the degrees of plastid reduction in specific lineages. We show that the loss of the plastid genome is common and unexpectedly find many lineage- and species-specific plastid proteins, suggesting the presence of evolutionary innovations and neofunctionalizations that may confer new functional and metabolic capabilities that are yet to be discovered in these enigmatic organelles.
- Keywords
- apicomplexans, organelle evolution, parasites, plastids, reductive evolution,
- MeSH
- Photosynthesis genetics MeSH
- Phylogeny MeSH
- Metabolic Networks and Pathways MeSH
- Plastids * genetics MeSH
- Proteome * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Proteome * MeSH
The loss of mitochondria in oxymonad protists has been associated with the redirection of the essential Fe-S cluster assembly to the cytosol. Yet as our knowledge of diverse free-living protists broadens, the list of functions of their mitochondrial-related organelles (MROs) expands. We revealed another such function in the closest oxymonad relative, Paratrimastix pyriformis, after we solved the proteome of its MRO with high accuracy, using localization of organelle proteins by isotope tagging (LOPIT). The newly assigned enzymes connect to the glycine cleavage system (GCS) and produce folate derivatives with one-carbon units and formate. These are likely to be used by the cytosolic methionine cycle involved in S-adenosyl methionine recycling. The data provide consistency with the presence of the GCS in MROs of free-living species and its absence in most endobionts, which typically lose the methionine cycle and, in the case of oxymonads, the mitochondria.
- Keywords
- LOPIT, Paratrimastix, glycine cleavage system, methionine cycle, mitochondrion-related organelle, one-carbon metabolism, proteome, spatial proteomics,
- MeSH
- Eukaryota metabolism MeSH
- Methionine * MeSH
- Mitochondria * metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Methionine * MeSH
Eukaryotic organelles supposedly evolved from their bacterial ancestors because of their benefits to host cells. However, organelles are quite often retained, even when the beneficial metabolic pathway is lost, due to something other than the original beneficial function. The organellar function essential for cell survival is, in the end, the result of organellar evolution, particularly losses of redundant metabolic pathways present in both the host and endosymbiont, followed by a gradual distribution of metabolic functions between the organelle and host. Such biological division of metabolic labor leads to mutual dependence of the endosymbiont and host. Changing environmental conditions, such as the gradual shift of an organism from aerobic to anaerobic conditions or light to dark, can make the original benefit useless. Therefore, it can be challenging to deduce the original beneficial function, if there is any, underlying organellar acquisition. However, it is also possible that the organelle is retained because it simply resists being eliminated or digested untill it becomes indispensable.
- Keywords
- benefit, endosymbiosis, essential function, mitochondrion, organelle, plastid,
- Publication type
- Journal Article MeSH
- Review MeSH
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.
Plastids are membrane-bound organelles that bestow phototrophic abilities to eukaryotes [...].
- MeSH
- Biological Evolution MeSH
- Plastids * metabolism genetics MeSH
- Symbiosis * MeSH
- Publication type
- Introductory Journal Article MeSH
- Editorial MeSH
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.
- Keywords
- apical complex, attachment, epimerite, feeder organelle, mucron, myzocytosis, nutrition, parasitophorous vacuole/sac, pores, trophozoite,
- Publication type
- Journal Article MeSH
- Review MeSH
