Biology subjects

Ros-Rocher, N.

Publications and source records attributed to Ros-Rocher, N..

5 recordsLinked to original sources

bioRxiv2024

Exogenous lipid vesicles induce endocytosis-mediated cellular aggregation in a close unicellular relative of animals

Capsaspora owczarzaki is a protozoan that may both reveal aspects of animal evolution and also curtail the spread of schistosomiasis, a neglected tropical disease. Capsaspora exhibits a chemically regulated aggregative behavior that resembles cellular aggregation in some animals. This behavior may have played a key role in the evolution of animal multicellularity. Additionally, this aggregative behavior may be important for Capsasporas ability to colonize the intermediate host of parasitic schistosomes and potentially prevent the spread of schistosomiasis. Both applications demand elucidation of the molecular mechanism of Capsaspora aggregation. Toward this goal, we first determined the necessary chemical properties of lipid cues that activate aggregation. We found that a wide range of abundant zwitterionic lipids induced aggregation, revealing that the aggregative behavior could be activated by diverse lipid-rich conditions. Furthermore, we demonstrated that aggregation in Capsaspora requires clathrin-mediated endocytosis, highlighting the potential significance of endocytosis-linked cellular signaling in recent animal ancestors. Finally, we found that aggregation was initiated by post-translational activation of cell-cell adhesion--not transcriptional regulation of cellular adhesion machinery. Our findings illuminate the chemical, molecular and cellular mechanisms that regulate Capsaspora aggregative behavior--with implications for the evolution of animal multicellularity and the transmission of parasites.

biochemistry↗

bioRxiv2024

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Multicellularity evolved multiple times independently during eukaryotic diversification1-4. Two distinct mechanisms underpin multicellularity5: clonality (serial cell division without sister-cell separation) and aggregation (whereby independent cells assemble into a multicellular entity). Clonal and aggregative multicellularity are traditionally considered mutually exclusive1,6-9, with rare exceptions10, and evolutionary hypotheses have addressed why multicellularity might diverge toward one or the other extreme3,4. Both animals and their sister group, the choanoflagellates, are currently only known to acquire multicellularity clonally4,11-13. Here, we show that the choanoflagellate Choanoeca flexa14 forms motile and contractile cell monolayers (or "sheets") through multiple mechanisms: C. flexa sheets can form purely clonally, purely aggregatively, or by a combination of both processes. We characterise the life history of C. flexa in its natural environment - ephemeral splash pools on the island of Curacao - and show that C. flexa undergoes reversible transitions between unicellularity and multicellularity during cycles of evaporation and refilling. Different splash pools house genetically distinct strains of C. flexa, between which aggregation is constrained by kin recognition15-18. We show that clonal-aggregative multicellularity serves as a versatile strategy for the robust re-establishment of multicellularity in this variable and fast-fluctuating environment. Our findings challenge former generalisations about choanoflagellates and expand the option space of choanozoan multicellularity.

evolutionary biology↗

bioRxiv2024

Host lipids regulate multicellular behavior of a predator of a human pathogen

As symbionts of animals, microbial eukaryotes benefit and harm their hosts in myriad ways. A model microeukaryote (Capsaspora owczarzaki) is a symbiont of Biomphalaria glabrata snails and may prevent transmission of parasitic schistosomes from snails to humans. However, it is unclear which host factors determine Capsasporas ability to colonize snails. Here, we discovered that Capsaspora forms multicellular aggregates when exposed to snail hemolymph. We identified a molecular cue for aggregation: a hemolymph-derived phosphatidylcholine, which becomes elevated in schistosome-infected snails. Therefore, Capsaspora aggregation may be a response to the physiological state of its host, and it may determine its ability to colonize snails and exclude parasitic schistosomes. Furthermore, Capsaspora is an evolutionary model organism whose aggregation may be ancestral to animals. This discovery, that a prevalent lipid induces Capsaspora multicellularity, suggests that this aggregation phenotype may be ancient. Additionally, the specific lipid will be a useful tool for further aggregation studies.

biochemistry↗

bioRxiv2023

PCP components control anterior and posterior regeneration, with a Prickle homolog impacting muscle organization, in the acoel Hofstenia miamia

Whole-body regeneration requires wound response signals to control patterning programs to enable replacement of structures in their correct locations. While a number of molecular mechanisms underlying anterior-posterior regeneration have been identified, how small fragments of animals first re-establish polarity is less well understood, with non-canonical Wnt signaling recently emerging as a potential regulator. Here, we used the acoel worm Hofstenia miamia, a new research organism capable of robust whole-body regeneration, to assess functions of the components of the Planar Cell Polarity (PCP) pathway in establishing regeneration polarity. We identified homologs of Prickle (pk-1) and Diego (dgo-1) to be required for head and tail regeneration, respectively. RNA-sequencing analysis and experimental corroboration revealed that pk-1 RNAi resulted in diminished expression of early wound response genes as well as of wound-induced expression of the anterior-specific marker fz-7, specifically in tail fragments. In contrast, dgo-1 RNAi impacted wound-induced expression of the posterior-specific marker tf7l2, specifically in head fragments. Furthermore, pk-1 and dgo-1 are enriched in longitudinal muscle, with muscle fibers showing disorganized morphology at anterior-facing wound sites of tail fragments under pk-1 RNAi. These findings suggest that pk-1 and dgo-1 are needed for wound-induced expression of anterior- and posterior-specific genes, and raise the possibility that this action is mediated via the control of muscle fiber orientation. Our work expands the study of PCP genes by revealing their functions in the process of whole-body regeneration in acoels, the sister-group to all other animals with bilateral symmetry, and will enable future studies of PCP components in controlling cellular and tissue-wide regeneration polarity.

developmental biology↗

bioRxiv2022

Chemical factors induce aggregative multicellularity in a close unicellular relative of animals

Regulated cellular aggregation is an essential process for development and healing in many animal tissues. In some animals and a few distantly related unicellular species, cellular aggregation is regulated by diffusible chemical cues. However, it is unclear whether regulated cellular aggregation was part of the life cycles of the first multicellular animals and/or their unicellular ancestors. To fill this gap, we investigated the triggers of cellular aggregation in one of animals closest unicellular living relatives - the filasterean Capsaspora owczarzaki. We discovered that Capsaspora aggregation is induced by chemical cues, as observed in some of the earliest branching animals and other unicellular species. Specifically, we found that calcium ions and lipids present in lipoproteins function together to induce aggregation of viable Capsaspora cells. We also found that this multicellular stage is reversible, as depletion of the cues triggers disaggregation, which can be overcome upon re-induction. Our finding demonstrates that chemically regulated aggregation is important across diverse members of the holozoan clade. Therefore, this phenotype was plausibly integral to the life cycles of the unicellular ancestors of animals.

biochemistry↗