Capsaspora owczarzaki

Ferrer-Bonet, Maria; Ruiz‐Trillo, Iñaki

doi:10.1016/j.cub.2017.05.074

Cited by 27 publications

(27 citation statements)

References 5 publications

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“…Moreover, both species have demonstrably experienced gene loss, as some genes conserved among animals and non-choanoflagellates are apparently missing from M. brevicollis and S. rosetta . Examples include RNAi pathway components, which are present across eukaryotes ( Shabalina and Koonin, 2008 ), the cell adhesion protein β-integrin, and T-box and Runx transcription factor families, which have been detected in the filasterean Capsaspora owczarzaki ( Sebé-Pedrós and Ruiz-Trillo, 2010 ; Sebé-Pedrós et al, 2010 ; Sebé-Pedrós et al, 2011 ; Sebé-Pedrós et al, 2013a ; Ferrer-Bonet and Ruiz-Trillo, 2017 ). Gene loss can lead to false negatives during ancestral genome reconstruction, and the phenomenon in choanoflagellates parallels that of animals, where two species selected for early genome projects, Drosophila melanogaster and Caenorhabditis elegans , were later found to have lost numerous genes (e.g., Hedgehog and NF-κΒ in C. elegans and fibrillar collagens in both C. elegans and D. melanogaster ) that are critical for animal development and otherwise conserved across animal diversity ( C. elegans Sequencing Consortium, 1998 ; Aspöck et al, 1999 ; Gilmore, 1999 ; Rubin et al, 2000 ).…”

Section: Introductionmentioning

confidence: 99%

Gene family innovation, conservation and loss on the animal stem lineage

Richter

Fozouni

Eisen

et al. 2018

eLife

184

300

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Choanoflagellates, the closest living relatives of animals, can provide unique insights into the changes in gene content that preceded the origin of animals. However, only two choanoflagellate genomes are currently available, providing poor coverage of their diversity. We sequenced transcriptomes of 19 additional choanoflagellate species to produce a comprehensive reconstruction of the gains and losses that shaped the ancestral animal gene repertoire. We identified ~1944 gene families that originated on the animal stem lineage, of which only 39 are conserved across all animals in our study. In addition, ~372 gene families previously thought to be animal-specific, including Notch, Delta, and homologs of the animal Toll-like receptor genes, instead evolved prior to the animal-choanoflagellate divergence. Our findings contribute to an increasingly detailed portrait of the gene families that defined the biology of the Urmetazoan and that may underpin core features of extant animals.

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Section: Introductionmentioning

confidence: 99%

Gene family innovation, conservation and loss on the animal stem lineage

Richter

Fozouni

Eisen

et al. 2018

eLife

184

300

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“…This filopodial amoeba is a facultative endosymbiont (Harcet et al 2016) isolated from explanted pericardial sacs of laboratory-grown Biomphalaria sp. snails (Stibbs et al 1979;Morgan et al 2002), which remains elusive in environmental samplings (Hertel et al 2004;del Campo and Ruiz-Trillo 2013;Shanan et al 2015;Ferrer-Bonet and Ruiz-Trillo 2017;Arroyo et al 2018). In contrast, the other four species (Ministeria vibrans, Ministeria marisola, Pigoraptor chileana, and Pigoraptor vietnamica) are free-living flagellates, sampled from marine and freshwater ecosystems (Patterson et al 1993;Tong et al 1997;Hehenberger et al 2017;Mylnikov et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Txikispora philomaiosn. sp., n. g., a Micro-Eukaryotic Pathogen of Amphipods, Reveals Parasitism and Hidden Diversity in Class Filasterea

Urrutia

Mitsi

Foster

et al. 2021

Preprint

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This study provides a morphological, ultrastructural, and phylogenetic characterization of a novel micro-eukaryotic parasite (2.3-2.6 µm) infecting genera Echinogammarus and Orchestia. Longitudinal studies across two years revealed that infection prevalence peaked in late April and May, reaching 64% in Echinogammarus sp. and 15% in Orchestia sp., but was seldom detected during the rest of the year. The parasite infected predominantly haemolymph, connective tissue, tegument, and gonad, although hepatopancreas and nervous tissue were affected in heavier infections, eliciting melanization and granuloma formation. Cell division occurred inside walled parasitic cysts, often within host haemocytes, resulting in haemolymph congestion. Small subunit (18S) rRNA gene phylogenies including related environmental sequences placed the novel parasite as a highly divergent lineage within Class Filasterea, which together with Choanoflagellatea represent the closest protistan relatives of Metazoa. We describe the new parasite as Txikispora philomaios n. sp. n. g., the first confirmed parasitic filasterean lineage, which otherwise comprises four free-living flagellates and a rarely observed endosymbiont of snails. Lineage-specific PCR probing of other hosts and surrounding environments only detected T. philomaios in the platyhelminth Procerodes sp. We expand the known diversity of Filasterea by targeted searches of metagenomic datasets, resulting in 13 previously unknown lineages from environmental samples.

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“…Thus, we sought to investigate the cell cycle control in another organism within opisthokonts that has retained the ancestral cell cycle regulation. We focused on Capsaspora owczarzaki (hereafter Capsaspora ), a species more closely related to animals than yeasts, easy to culture, and for which good genomic resources are available [56–59]. This amoeba has a life cycle that includes three distinct stages that differ both in their morphology and transcriptional and proteomic profiles: amoebas with filopodia that proliferate in adherent cultures, an aggregative multicellular stage in which cells produce an extracellular matrix, and a cystic form that lacks filopodia [60–62].…”

Section: Introductionmentioning

confidence: 99%

Gradual evolution of cell cycle regulation by cyclin-dependent kinases during the transition to animal multicellularity

Pérez-Posada

Dudin

Ocaña‐Pallarès

et al. 2019

Preprint

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Progression through the cell cycle in eukaryotes is regulated on multiple levels. The main driver of the cell cycle progression is the periodic activity of cyclin-dependent kinase (CDK) complexes. In parallel, transcription during the cell cycle is regulated by a transcriptional program that ensures the just-in-time gene expression. Many core cell cycle regulators are present in all eukaryotes, among them cyclins and CDKs; however, periodic transcriptional programs are divergent between distantly related species. In addition, many otherwise conserved cell cycle regulators have been lost and independently evolved in yeast, a widely used model organism for cell cycle research. To gain insight into the cell cycle regulation in a more representative opisthokont, we investigated the cell cycle regulation at the transcriptional level of Capsaspora owczarzaki, a species closely related to animals. We developed a protocol for cell cycle synchronization in Capsaspora cultures and assessed gene expression over time across the entire cell cycle. We identified a set of 801 periodic genes that grouped into five clusters of expression over time. Comparison with datasets from other eukaryotes revealed that the periodic transcriptional program of Capsaspora is most similar to that of animal cells. We found that orthologues of cyclin A, B and E are expressed at the same cell cycle stages as in human cells and in the same temporal order. However, in contrast to human cells where these cyclins interact with multiple CDKs, Capsaspora cyclins likely interact with a single ancestral CDK1-3. Thus, the Capsaspora cyclin-CDK system could represent an intermediate state in the evolution of animal-like cyclin-CDK regulation. Overall, our results demonstrate that Capsaspora could be a useful unicellular model system for animal cell cycle regulation.Author’s summaryWhen cells reproduce, proper duplication and splitting of the genetic material is ensured by cell cycle control systems. Many of the regulators in these systems are present across all eukaryotes, such as cyclin and cyclin-dependent kinases (CDK), or the E2F-Rb transcriptional network. Opisthokonts, the group comprising animals, yeasts and their unicellular relatives, represent a puzzling scenario: in contrast to animals, where the cell cycle core machinery seems to be conserved, studies in yeasts have shown that some of these regulators have been lost and independently evolved. For a better understanding of the evolution of the cell cycle regulation in opisthokonts, and ultimately in the lineage leading to animals, we have studied cell cycle regulation in Capsaspora owczarzaki, a unicellular amoeba more closely related to animals than fungi that retains the ancestral cell cycle toolkit. Our findings suggest that, in the ancestor of Capsaspora and animals, cyclins oscillate in the same temporal order as in animals, and that expansion of CDKs occurred later in the lineage that led to animals.

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Capsaspora owczarzaki

Abstract: Capsaspora owczarzaki is a unicellular eukaryote that is becoming pivotal to understanding the origin of animal multicellularity.

Cited by 27 publications

References 5 publications

Gene family innovation, conservation and loss on the animal stem lineage

Gene family innovation, conservation and loss on the animal stem lineage

Txikispora philomaiosn. sp., n. g., a Micro-Eukaryotic Pathogen of Amphipods, Reveals Parasitism and Hidden Diversity in Class Filasterea

Gradual evolution of cell cycle regulation by cyclin-dependent kinases during the transition to animal multicellularity

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