Parallel functional reduction in the mitochondria of apicomplexan parasites

Mathur, Varsha; Wakeman, Kevin C.; Keeling, Patrick J.

doi:10.1016/j.cub.2021.04.028

Cited by 41 publications

(42 citation statements)

References 74 publications

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“…GUIDANCE2 alignment tends to place the Trichotokara+Paralecudina clade in the Ancoroidea, while the manually masked alignment brings these groups closer together only if using a BI under the CAT model (PhyloBayes tree), which is most free from the artifact of long branch attraction, or if excluding the most divergent sequences from the alignment (65 OUT tree). This is consistent with a recent multigene analysis of Trichotokara as a sister group to Ancoroidea (Mathur, Wakeman & Keeling, 2021). Generally, the GUIDANCE2 strategy showed less stable results than the structural alignment utilizing the X-INS-i algorithm, in particular with regard to placement of the Trichotokara and Paralecudina clade as well as the Cephaloidophora and Trollidiidae clades.…”

Section: The Resurrected Family Polyrhabdinidae and The Emended Superfamily Ancoroideasupporting

confidence: 89%

“…Additionally, the recent protein multigene phylogeny also revealed the affiliation of P. pygospionis (Polyrhabdina sp. in original) with Ancoroidea (Janouškovec et al, 2019;Mathur, Wakeman & Keeling, 2021). We conclude that the clade including P. pygospionis can be identified as the family Polyrhabdinidae Kamm, 1922, a taxon that should be re-established with a diagnosis emended by new morphological evidence (see Taxonomic summary).…”

Section: The Resurrected Family Polyrhabdinidae and The Emended Superfamily Ancoroideamentioning

confidence: 86%

“…However, recent studies that used the concatenated sequences of SSU and large subunit (LSU) rDNA genes have recovered relationships within Apicomplexa with a resolution superior to the analyses inferred from SSU rDNA alone and revealed gregarines as monophyletic (Paskerova et al, 2018;Simdyanov, Diakin & Aleoshin, 2015;Simdyanov et al, 2017;Simdyanov et al, 2018). This conclusion was unambiguously supported by phylogenetic analyses based on 296 (Janouškovec et al, 2019) and 195 (Mathur, Wakeman & Keeling, 2021) concatenated protein-coding genes. The observation that concatenated rDNA sequences perform better at resolving deep phylogenetic relationships in a group than SSU rDNA alone is receiving increasing support in studies of protist diversity (Jamy et al, 2019).…”

Section: Introductionmentioning

confidence: 96%

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Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation

Paskerova

Miroliubova

Valigurová

et al. 2021

PeerJ

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Background Gregarines are a major group of apicomplexan parasites of invertebrates. The gregarine classification is largely incomplete because it relies primarily on light microscopy, while electron microscopy and molecular data in the group are fragmentary and often do not overlap. A key characteristic in gregarine taxonomy is the structure and function of their attachment organelles (AOs). AOs have been commonly classified as “mucrons” or “epimerites” based on their association with other cellular traits such as septation. An alternative proposal focused on the AOs structure, functional role, and developmental fate has recently restricted the terms “mucron” to archigregarines and “epimerite” to eugregarines. Methods Light microscopy and scanning and transmission electron microscopy, molecular phylogenetic analyses of ribosomal RNA genes. Results We obtained the first data on fine morphology of aseptate eugregarines Polyrhabdina pygospionis and Polyrhabdina cf. spionis, the type species. We demonstrate that their AOs differ from the mucron in archigregarines and represent an epimerite structurally resembling that in other eugregarines examined using electron microscopy. We then used the concatenated ribosomal operon DNA sequences (SSU, 5.8S, and LSU rDNA) of P. pygospionis to explore the phylogeny of eugregarines with a resolution superior to SSU rDNA alone. The obtained phylogenies show that the Polyrhabdina clade represents an independent, deep-branching family in the Ancoroidea clade within eugregarines. Combined, these results lend strong support to the hypothesis that the epimerite is a synapomorphic innovation of eugregarines. Based on these findings, we resurrect the family Polyrhabdinidae Kamm, 1922 and erect and diagnose the family Trollidiidae fam. n. within the superfamily Ancoroidea Simdyanov et al., 2017. Additionally, we re-describe the characteristics of P. pygospionis, emend the diagnoses of the genus Polyrhabdina, the family Polyrhabdinidae, and the superfamily Ancoroidea.

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Section: The Resurrected Family Polyrhabdinidae and The Emended Superfamily Ancoroideasupporting

confidence: 89%

Section: The Resurrected Family Polyrhabdinidae and The Emended Superfamily Ancoroideamentioning

confidence: 86%

Section: Introductionmentioning

confidence: 96%

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Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation

Paskerova

Miroliubova

Valigurová

et al. 2021

PeerJ

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“…Emerging data based on single-cell genomics of apicomplexan groups suggests that the currently accepted phylum, encompassing over 6,000 species, could actually be polyphyletic (Janouškovec et al, 2019;Mathur et al, 2021). In light of these results, it has been put forward that morphological similarities could have evolved convergently at least three times.…”

Section: Phylogeny Of the Phylum Apicomplexamentioning

confidence: 99%

“…Finally, the cyrptosporidians include all Cryptosporidium species; C. hominis, C. parvum, C. muris, among others. Recently, transcriptomic data allowed the assessment of the divergence pattern involving coccidiomorphs, gregarines and cryptosporidians and results support the placement of Cryptosporidium as the earliest diverging lineage of apicomplexans (Mathur et al, 2021;Salomaki et al, 2021). However, the history of early apicomplexan radiation remains highly contentious (Janouškovec et al, 2019;Mathur et al, 2019Mathur et al, , 2021Salomaki et al, 2021), which impacts our interpretation of evolutionary events within the phylum.…”

Section: Phylogeny Of the Phylum Apicomplexamentioning

confidence: 99%

The Elusive Mitochondrial Genomes of Apicomplexa: Where Are We Now?

2021

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Mitochondria are vital organelles of eukaryotic cells, participating in key metabolic pathways such as cellular respiration, thermogenesis, maintenance of cellular redox potential, calcium homeostasis, cell signaling, and cell death. The phylum Apicomplexa is entirely composed of obligate intracellular parasites, causing a plethora of severe diseases in humans, wild and domestic animals. These pathogens include the causative agents of malaria, cryptosporidiosis, neosporosis, East Coast fever and toxoplasmosis, among others. The mitochondria in Apicomplexa has been put forward as a promising source of undiscovered drug targets, and it has been validated as the target of atovaquone, a drug currently used in the clinic to counter malaria. Apicomplexans present a single tubular mitochondria that varies widely both in structure and in genomic content across the phylum. The organelle is characterized by massive gene migrations to the nucleus, sequence rearrangements and drastic functional reductions in some species. Recent third generation sequencing studies have reignited an interest for elucidating the extensive diversity displayed by the mitochondrial genomes of apicomplexans and their intriguing genomic features. The underlying mechanisms of gene transcription and translation are also ill-understood. In this review, we present the state of the art on mitochondrial genome structure, composition and organization in the apicomplexan phylum revisiting topological and biochemical information gathered through classical techniques. We contextualize this in light of the genomic insight gained by second and, more recently, third generation sequencing technologies. We discuss the mitochondrial genomic and mechanistic features found in evolutionarily related alveolates, and discuss the common and distinct origins of the apicomplexan mitochondria peculiarities.

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How mitochondrial cristae illuminate the important role of oxygen during eukaryogenesis

Speijer

2024

BioEssays

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Inner membranes of mitochondria are extensively folded, forming cristae. The observed overall correlation between efficient eukaryotic ATP generation and the area of internal mitochondrial inner membranes both in unicellular organisms and metazoan tissues seems to explain why they evolved. However, the crucial use of molecular oxygen (O2) as final acceptor of the electron transport chain is still not sufficiently appreciated. O2 was an essential prerequisite for cristae development during early eukaryogenesis and could be the factor allowing cristae retention upon loss of mitochondrial ATP generation. Here I analyze illuminating bacterial and unicellular eukaryotic examples. I also discuss formative influences of intracellular O2 consumption on the evolution of the last eukaryotic common ancestor (LECA). These considerations bring about an explanation for the many genes coming from other organisms than the archaeon and bacterium merging at the start of eukaryogenesis.

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Parallel functional reduction in the mitochondria of apicomplexan parasites

Cited by 41 publications

References 74 publications

Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation

Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation

The Elusive Mitochondrial Genomes of Apicomplexa: Where Are We Now?

How mitochondrial cristae illuminate the important role of oxygen during eukaryogenesis

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