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Arielle Woznica - One of the best experts on this subject based on the ideXlab platform.
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Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate.
Applied and Environmental Microbiology, 2020Co-Authors: Ella V. Ireland, Arielle WoznicaAbstract:Bacteria regulate the life histories of diverse eukaryotes, but relatively little is known about how eukaryotes interpret and respond to multiple bacterial cues encountered simultaneously. To explore how a eukaryote might respond to a combination of bioactive molecules from multiple bacteria, we treated the choanoflagellate Salpingoeca rosetta with two sets of bacterial cues, one that induces mating and another that induces multicellular development. We found that simultaneous exposure to both sets of cues enhanced multicellular development in S. rosetta, eliciting both larger multicellular colonies and an increase in the number of colonies. Thus, rather than conveying conflicting sets of information, these distinct bacterial cues synergize to augment multicellular development. This study demonstrates how a eukaryote can integrate and modulate its response to cues from diverse bacteria, underscoring the potential impact of complex microbial communities on eukaryotic life histories.IMPORTANCE Eukaryotic biology is profoundly influenced by interactions with diverse environmental and host-associated bacteria. However, it is not well understood how eukaryotes interpret multiple bacterial cues encountered simultaneously. This question has been challenging to address because of the complexity of many eukaryotic model systems and their associated bacterial communities. Here, we studied a close relative of animals, the choanoflagellate Salpingoeca rosetta, to explore how eukaryotes respond to diverse bacterial cues. We found that a bacterial chondroitinase that induces mating on its own can also synergize with bacterial lipids that induce multicellular "rosette" development. When encountered together, these cues enhance rosette development, resulting in both the formation of larger rosettes and an increase in the number of rosettes compared to rosette development in the absence of the chondroitinase. These findings highlight how synergistic interactions among bacterial cues can influence the biology of eukaryotes.
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Synergistic cues from diverse bacteria enhance multicellular development in a choanoflagellate
bioRxiv, 2019Co-Authors: Ella V. Ireland, Arielle WoznicaAbstract:Abstract Bacteria regulate the life histories of diverse eukaryotes, but relatively little is known about how eukaryotes interpret and respond to multiple bacterial cues encountered simultaneously. To explore how a eukaryote might respond to a combination of bioactive molecules from multiple bacteria, we treated the choanoflagellate Salpingoeca rosetta with two sets of bacterial cues, one that induces mating and the other that induces multicellular development. We found that simultaneous exposure to both sets of cues enhanced multicellular development in S. rosetta, eliciting both larger multicellular colonies and an increase in the number of colonies. Thus, rather than conveying conflicting sets of information, these distinct bacterial cues synergize to augment multicellular development. This study demonstrates how a eukaryote can integrate and modulate its response to cues from diverse bacteria, underscoring the potential impact of complex microbial communities on eukaryotic life histories. Importance Eukaryotic biology is profoundly influenced by interactions with diverse environmental and host-associated bacteria. However, it is not well understood how eukaryotes interpret multiple bacterial cues encountered simultaneously. This question has been challenging to address because of the complexity of many eukaryotic model systems and their associated bacterial communities. Here, we studied a close relative of animals, the choanoflagellate Salpingoeca rosetta, to explore how eukaryotes respond to diverse bacterial cues. We found that a bacterial chondroitinase that induces mating on its own can also synergize with bacterial lipids that induce multicellular “rosette” development. When encountered together, these cues enhance rosette development, resulting in the formation of more rosettes, each containing more cells than rosettes that form in the absence of the chondroitinase. These findings highlight how synergistic interactions among bacterial cues can influence the biology of eukaryotes.
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Bacterial cues regulate multicellular development and mating in the choanoflagellate, S. rosetta
2017Co-Authors: Arielle WoznicaAbstract:Author(s): Woznica, Arielle | Advisor(s): King, Nicole | Abstract: Animals first diverged from their unicellular ancestors in oceans dominated by bacteria, and have lived in close association with bacteria ever since. Interactions with bacteria critically shape diverse aspects of animal biology today, including developmental processes that were long thought to be autonomous. Yet, the multicellularity of animals and the often-complex communities of bacteria with which they are associated make it challenging to characterize the mechanisms underlying many bacterial-animal interactions. Thus, developing experimentally tractable host-microbe model systems will be essential for revealing the molecules and mechanisms by which bacteria influence animal development. The choanoflagellate Salpingoeca rosetta, one of the closest living relatives of animals, has emerged as an attractive model for studying host-microbe interactions. Like all choanoflagellates, S. rosetta feeds on bacteria; however, we have found that interactions between S. rosetta and bacteria extend beyond those of predator and prey. In fact, two key transitions in the life history of S. rosetta, multicellular “rosette” development and sexual reproduction, are regulated by environmental bacteria. The experimental tractability of S. rosetta allowed us to characterize the molecules and regulatory logic underpinning the bacterial regulation of rosette development (Chapters 2 and 3). We found that the bacterium Algoriphagus machipongonensis produces three classes of structurally distinct lipids that are interpreted by S. rosetta as activators, synergistic enhancers, and inhibitors of rosette development. Although activating sulfonolipid RIFs (Rosette Inducing Factors) elicited relatively low levels of rosette development, the combined activity of the RIFs and synergizing lysophosphatidylethanolamines (LPEs; which alone had no detectable activity) was sufficient to fully recapitulate the rosette-inducing activity of Algoriphagus bacteria. Moreover, we identified a potent antagonist of the RIFs, IOR-1 (Inhibitor of Rosettes), but found that the synergistic activities of the RIFs and the LPEs overcame the inhibitory activities of IOR-1. We hypothesize that the integration of multiple activating, enhancing, and inhibitory bacterial cues act to ensure that rosette development is not initiated under the wrong environmental conditions. Until recently, bacteria were not known to influence any life history transition in S. rosetta other than rosette development. We serendipitously discovered that the bacterium Vibrio fischeri produces an “aphrodisiac” that regulates sexual reproduction in S. rosetta (Chapter 4). To our knowledge, the interaction between Vibrio and S. rosetta is the first known example of bacteria regulating mating in a eukaryote. After observing that S. rosetta cells aggregate into large swarms in response to Vibrio bacteria, we demonstrated that swarming, a behavior that had not been previously observed in choanoflagellates, was a prelude to sexual fusion. We next found that Vibrio secreted a chondroitinase aphrodisiac (EroS) that depolymerized chondroitin sulfate, a glycosaminoglycan previously thought to be restricted to animals, in the S. rosetta extracellular matrix. Finally, we determined mating in S. rosetta was triggered by low cell densities of Vibrio bacteria, and picomolar concentrations of EroS (as well as other bacterial chondroitinases), indicating that bacteria could plausibly trigger S. rosetta swarming and mating in the environment. We predict that the presence of chondroitinase-producing bacteria may indicate environmental factors that favor mating in S. rosetta.
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An Aphrodisiac Produced By Vibrio fischeri Stimulates Mating In The Closest Living Relatives Of Animals
bioRxiv, 2017Co-Authors: Arielle Woznica, Joseph P. Gerdt, Ryan E. Hulett, Jon ClardyAbstract:We serendipitously discovered that the marine bacterium Vibrio fischeri induces sexual reproduction in one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta . Although bacteria influence everything from nutrition and metabolism to cell biology and development in eukaryotes, bacterial regulation of eukaryotic mating was unexpected. Here we show that a single V. fischeri protein, the previously uncharacterized EroS, fully recapitulates the aphrodisiac activity of live V. fischeri . EroS is a chondroitin lyase; although its substrate, chondroitin sulfate, was previously thought to be an animal synapomorphy, we demonstrate that S. rosetta produces chondroitin sulfate and thus extend the ancestry of this important glycosaminoglycan to the premetazoan era. Finally, we show that V. fischeri , purified EroS, and other bacterial chondroitin lyases induce S. rosetta mating at environmentally-relevant concentrations suggesting that bacterially-produced aphrodisiacs likely regulate choanoflagellate mating in nature.
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Synthesis of the Rosette-Inducing Factor RIF‑1 and Analogs
2016Co-Authors: Christine Beemelmanns, Rosanna A. Alegado, Arielle Woznica, Ra M. Cantley, Jon ClardyAbstract:ABSTRACT: Studies on the origin of animal multi-cellularity have increasingly focused on one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta. Single cells of S. rosetta can develop into multicellular rosette-shaped colonies through a process of incomplete cytokinesis. Unexpectedly, the initiation of rosette development requires bacterially produced small molecules. Previously, our laboratories reported the planar structure and femtomolar rosette-inducing activity of one rosette-inducing small molecule, dubbed rosette-inducing factor 1 (RIF-1), produced by the Gram-negative Bacteroidetes bacterium Algoriphagus machipongonensis. RIF-1 belongs to the small and poorly explored class of sulfonolipids. Here, we report a modular total synthesis of RIF-1 stereoisomers and structural analogs. Rosette
Pawel Burkhardt - One of the best experts on this subject based on the ideXlab platform.
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Spatial Cell Disparity in the Colonial Choanoflagellate Salpingoeca rosetta.
Frontiers in Cell and Developmental Biology, 2019Co-Authors: Benjamin Naumann, Pawel BurkhardtAbstract:Choanoflagellates are the closest unicellular relatives of animals (Metazoa). These tiny protists display complex life histories that include sessile as well as different pelagic stages. Some choanoflagellates have the ability to form colonies as well. Up until recently, these colonies have been described to consist of mostly identical cells showing no spatial cell differentiation, which supported the traditional view that spatial cell differentiation, leading to the co-existence of specific cell types in animals, evolved after the split of the last common ancestor of the Choanoflagellata and Metazoa. The recent discovery of single cells in colonies of the choanoflagellate Salpingoeca rosetta that exhibit unique cell morphologies challenges this traditional view. We have now reanalyzed TEM serial sections, aiming to determine the degree of similarity of S. rosetta cells within a rosette colony. We investigated cell morphologies and nuclear, mitochondrial, and food vacuole volumes of 40 individual cells from four different S. rosetta rosette colonies and compared our findings to sponge choanocytes. Our analysis shows that cells in a choanoflagellate colony differ from each other in respect to cell morphology and content ratios of nuclei, mitochondria, and food vacuoles. Furthermore, cell disparity within S. rosetta colonies is slightly higher compared to cell disparity within sponge choanocytes. Moreover, we discovered the presence of plasma membrane contacts between colonial cells in addition to already described intercellular bridges and filo-/pseudopodial contacts. Our findings indicate that the last common ancestor of Choanoflagellata and Metazoa might have possessed plasma membrane contacts and spatial cell disparity during colonial life history stages.
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Spatial cell disparity in the colonial choanoflagellate Salpingoeca rosetta
bioRxiv, 2019Co-Authors: Benjamin Naumann, Pawel BurkhardtAbstract:Abstract Choanoflagellates are the closest unicellular relatives of animals (Metazoa). These tiny protists display complex life histories that include sessile as well as different pelagic stages. Some choanoflagellates have the ability to form colonies as well. Up until recently, these colonies have been described to consist of mostly identical cells showing no spatial cell differentiation, which supported the traditional view that spatial cell differentiation, leading to specific cell types in animals, evolved after the split of the last common ancestor of the Choanoflagellata and Metazoa. The recent discovery of single cells in colonies of the choanoflagellate Salpingoeca rosetta that exhibit unique cell morphologies challenges this traditional view. We have now reanalyzed TEM serial sections, aiming to determine the degree of similarity of S. rosetta cells within a rosette colony. We investigated cell morphologies and nuclear, mitochondrial and food vacuole volumes of 40 individual cells from four different S. rosetta rosette colonies and compared our findings to previously published data on sponge choanocytes. Our analysis show that cells in a choanoflagellate colony differ from each other in respect to cell morphology and content ratios of nuclei, mitochondria and food vacuoles. Furthermore, cell disparity within S. rosetta colonies is higher compared to cell disparity within sponge choanocytes. Moreover, we discovered the presence of plasma membrane contacts between colonial cells in addition to already described intercellular bridges and filo-/pseudopodial contacts. Our findings indicate that the last common ancestor of Choanoflagellata and Metazoa might have possessed plasma membrane contacts and spatial cell disparity during colonial life history stages.
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The architecture of cell differentiation in choanoflagellates and sponge choanocytes.
PLOS Biology, 2019Co-Authors: Davis Laundon, Kent L. Mcdonald, Ben T. Larson, Pawel BurkhardtAbstract:Although collar cells are conserved across animals and their closest relatives, the choanoflagellates, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta expresses genes necessary for animal development and can alternate between unicellular and multicellular states, making it a powerful model for investigating the origin of animal multicellularity and mechanisms underlying cell differentiation. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular ‘rosette’ colonies and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with higher levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell–cell contact networks, and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type, pointing toward spatial cell differentiation. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some but not all neighbouring cells. Reconstruction of sponge choanocytes revealed ultrastructural commonalities but also differences in major organelle composition in comparison to choanoflagellates. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of animals.
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The architecture of cell differentiation in choanoflagellates and sponge choanocytes
bioRxiv, 2018Co-Authors: Davis Laundon, Nicole King, Kent L. Mcdonald, Ben T. Larson, Pawel BurkhardtAbstract:Collar cells are ancient animal cell types which are conserved across the animal kingdom and their closest relatives, the choanoflagellates. However, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta expresses genes necessary for animal multicellularity and development and can alternate between unicellular and multicellular states making it a powerful model to investigate the origin of animal multicellularity and mechanisms underlying cell differentiation. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular 9rosettes9 and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with relatively high levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell-cell contact networks and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some, but not all, neighbouring cells. Reconstruction of sponge choanocytes revealed both ultrastructural commonalities and differences in comparison to choanoflagellates. Choanocytes and colonial choanoflagellates are typified by high amoeboid cell activity. In both, the number of microvilli and volumetric proportion of the Golgi apparatus are comparable, whereas choanocytes devote less of their cell volume to the nucleus and mitochondria than choanoflagellates and more of their volume to food vacuoles. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of the animal kingdom.
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A rticle Fast T rack Insights into the Origin of Metazoan Filopodia and Microvilli
2016Co-Authors: Pawel Burkhardt, Franz B LangAbstract:Filopodia are fine actin-based cellular projections used for both environmental sensing and cell motility, and they are essential organelles for metazoan cells. In this study, we reconstruct the origin of metazoan filopodia and microvilli. We first report on the evolutionary assembly of the filopodial molecular toolkit and show that homologs of many metazoan filopodial components, including fascin and myosin X, were already present in the unicellular or colonial progenitors of metazoans. Furthermore, we find that the actin crosslinking protein fascin localizes to filopodia-like structures and microvilli in the choanoflagellate Salpingoeca rosetta. In addition, homologs of filopodial genes in the holozoan Capsaspora owczarzaki are upregulated in filopodia-bearing cells relative to those that lack them. Therefore, our findings suggest that proteins essential for metazoan filopodia and microvilli are functionally conserved in unicellular and colonial holozoans and that the last common ancestor of metazoans bore a complex and specific filopodial machinery
Jon Clardy - One of the best experts on this subject based on the ideXlab platform.
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An Aphrodisiac Produced By Vibrio fischeri Stimulates Mating In The Closest Living Relatives Of Animals
bioRxiv, 2017Co-Authors: Arielle Woznica, Joseph P. Gerdt, Ryan E. Hulett, Jon ClardyAbstract:We serendipitously discovered that the marine bacterium Vibrio fischeri induces sexual reproduction in one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta . Although bacteria influence everything from nutrition and metabolism to cell biology and development in eukaryotes, bacterial regulation of eukaryotic mating was unexpected. Here we show that a single V. fischeri protein, the previously uncharacterized EroS, fully recapitulates the aphrodisiac activity of live V. fischeri . EroS is a chondroitin lyase; although its substrate, chondroitin sulfate, was previously thought to be an animal synapomorphy, we demonstrate that S. rosetta produces chondroitin sulfate and thus extend the ancestry of this important glycosaminoglycan to the premetazoan era. Finally, we show that V. fischeri , purified EroS, and other bacterial chondroitin lyases induce S. rosetta mating at environmentally-relevant concentrations suggesting that bacterially-produced aphrodisiacs likely regulate choanoflagellate mating in nature.
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Synthesis of the Rosette-Inducing Factor RIF‑1 and Analogs
2016Co-Authors: Christine Beemelmanns, Rosanna A. Alegado, Arielle Woznica, Ra M. Cantley, Jon ClardyAbstract:ABSTRACT: Studies on the origin of animal multi-cellularity have increasingly focused on one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta. Single cells of S. rosetta can develop into multicellular rosette-shaped colonies through a process of incomplete cytokinesis. Unexpectedly, the initiation of rosette development requires bacterially produced small molecules. Previously, our laboratories reported the planar structure and femtomolar rosette-inducing activity of one rosette-inducing small molecule, dubbed rosette-inducing factor 1 (RIF-1), produced by the Gram-negative Bacteroidetes bacterium Algoriphagus machipongonensis. RIF-1 belongs to the small and poorly explored class of sulfonolipids. Here, we report a modular total synthesis of RIF-1 stereoisomers and structural analogs. Rosette
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bacterial lipids activate synergize and inhibit a developmental switch in choanoflagellates
Proceedings of the National Academy of Sciences of the United States of America, 2016Co-Authors: Arielle Woznica, Christine Beemelmanns, Alexandra M. Cantley, Elizaveta Freinkman, Jon ClardyAbstract:In choanoflagellates, the closest living relatives of animals, multicellular rosette development is regulated by environmental bacteria. The simplicity of this evolutionarily relevant interaction provides an opportunity to identify the molecules and regulatory logic underpinning bacterial regulation of development. We find that the rosette-inducing bacterium Algoriphagus machipongonensis produces three structurally divergent classes of bioactive lipids that, together, activate, enhance, and inhibit rosette development in the choanoflagellate Salpingoeca rosetta. One class of molecules, the lysophosphatidylethanolamines (LPEs), elicits no response on its own but synergizes with activating sulfonolipid rosette-inducing factors (RIFs) to recapitulate the full bioactivity of live Algoriphagus. LPEs, although ubiquitous in bacteria and eukaryotes, have not previously been implicated in the regulation of a host-microbe interaction. This study reveals that multiple bacterially produced lipids converge to activate, enhance, and inhibit multicellular development in a choanoflagellate.
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Isolation and Synthesis of a Bacterially Produced Inhibitor of Rosette Development in Choanoflagellates
Journal of the American Chemical Society, 2016Co-Authors: Alexandra M. Cantley, Arielle Woznica, Christine Beemelmanns, Jon ClardyAbstract:The choanoflagellate Salpingoeca rosetta is a microbial marine eukaryote that can switch between unicellular and multicellular states. As one of the closest living relatives of animals, this organism has become a model for understanding how multicellularity evolved in the animal lineage. Previously our laboratories isolated and synthesized a bacterially produced sulfonolipid that induces S. rosetta to form multicellular “rosettes.” In this study, we report the identification of a bacterially produced inhibitor of rosettes (IOR-1) as well as the total synthesis of this molecule and all of its stereoisomers. Our results confirm the previously noted specificity and potency of rosette-modulating molecules, expand our understanding of the complex chemical ecology between choanoflagellates and rosette-inducing bacteria, and provide a synthetic probe template for conducting further mechanistic studies on the emergence of multicellularity.
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Isolation and Synthesis of a Bacterially Produced Inhibitor of Rosette Development in Choanoflagellates
2016Co-Authors: Alexandra M. Cantley, Arielle Woznica, Christine Beemelmanns, Jon ClardyAbstract:The choanoflagellate Salpingoeca rosetta is a microbial marine eukaryote that can switch between unicellular and multicellular states. As one of the closest living relatives of animals, this organism has become a model for understanding how multicellularity evolved in the animal lineage. Previously our laboratories isolated and synthesized a bacterially produced sulfonolipid that induces S. rosetta to form multicellular “rosettes.” In this study, we report the identification of a bacterially produced inhibitor of rosettes (IOR-1) as well as the total synthesis of this molecule and all of its stereoisomers. Our results confirm the previously noted specificity and potency of rosette-modulating molecules, expand our understanding of the complex chemical ecology between choanoflagellates and rosette-inducing bacteria, and provide a synthetic probe template for conducting further mechanistic studies on the emergence of multicellularity
Martin Carr - One of the best experts on this subject based on the ideXlab platform.
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A genomic survey of transposable elements in the choanoflagellate Salpingoeca rosetta reveals selection on codon usage
Mobile DNA, 2019Co-Authors: Jade Southworth, Alan O. Marron, C. Alastair Grace, Nazeefa Fatima, Martin CarrAbstract:Background Unicellular species make up the majority of eukaryotic diversity, however most studies on transposable elements (TEs) have centred on multicellular host species. Such studies may have therefore provided a limited picture of how transposable elements evolve across eukaryotes. The choanoflagellates, as the sister group to Metazoa, are an important study group for investigating unicellular to multicellular transitions. A previous survey of the choanoflagellate Monosiga brevicollis revealed the presence of only three families of LTR retrotransposons, all of which appeared to be active. Salpingoeca rosetta is the second choanoflagellate to have its whole genome sequenced and provides further insight into the evolution and population biology of transposable elements in the closest relative of metazoans. Results Screening the genome revealed the presence of a minimum of 20 TE families. Seven of the annotated families are DNA transposons and the remaining 13 families are LTR retrotransposons. Evidence for two putative non-LTR retrotransposons was also uncovered, but full-length sequences could not be determined. Superfamily phylogenetic trees indicate that vertical inheritance and, in the case of one family, horizontal transfer have been involved in the evolution of the choanoflagellates TEs. Phylogenetic analyses of individual families highlight recent element activity in the genome, however six families did not show evidence of current transposition. The majority of families possess young insertions and the expression levels of TE genes vary by four orders of magnitude across families. In contrast to previous studies on TEs, the families present in S. rosetta show the signature of selection on codon usage, with families favouring codons that are adapted to the host translational machinery. Selection is stronger in LTR retrotransposons than DNA transposons, with highly expressed families showing stronger codon usage bias. Mutation pressure towards guanosine and cytosine also appears to contribute to TE codon usage. Conclusions S. rosetta increases the known diversity of choanoflagellate TEs and the complement further highlights the role of horizontal gene transfer from prey species in choanoflagellate genome evolution. Unlike previously studied TEs, the S. rosetta families show evidence for selection on their codon usage, which is shown to act via translational efficiency and translational accuracy.
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A genomic survey of transposable elements in the choanoflagellate Salpingoeca rosetta reveals selection on codon usage
Mobile Dna, 2019Co-Authors: Jade Southworth, Alan O. Marron, C. Alastair Grace, Nazeefa Fatima, Martin CarrAbstract:Unicellular species make up the majority of eukaryotic diversity, however most studies on transposable elements (TEs) have centred on multicellular host species. Such studies may have therefore provided a limited picture of how transposable elements evolve across eukaryotes. The choanoflagellates, as the sister group to Metazoa, are an important study group for investigating unicellular to multicellular transitions. A previous survey of the choanoflagellate Monosiga brevicollis revealed the presence of only three families of LTR retrotransposons, all of which appeared to be active. Salpingoeca rosetta is the second choanoflagellate to have its whole genome sequenced and provides further insight into the evolution and population biology of transposable elements in the closest relative of metazoans. Screening the genome revealed the presence of a minimum of 20 TE families. Seven of the annotated families are DNA transposons and the remaining 13 families are LTR retrotransposons. Evidence for two putative non-LTR retrotransposons was also uncovered, but full-length sequences could not be determined. Superfamily phylogenetic trees indicate that vertical inheritance and, in the case of one family, horizontal transfer have been involved in the evolution of the choanoflagellates TEs. Phylogenetic analyses of individual families highlight recent element activity in the genome, however six families did not show evidence of current transposition. The majority of families possess young insertions and the expression levels of TE genes vary by four orders of magnitude across families. In contrast to previous studies on TEs, the families present in S. rosetta show the signature of selection on codon usage, with families favouring codons that are adapted to the host translational machinery. Selection is stronger in LTR retrotransposons than DNA transposons, with highly expressed families showing stronger codon usage bias. Mutation pressure towards guanosine and cytosine also appears to contribute to TE codon usage. S. rosetta increases the known diversity of choanoflagellate TEs and the complement further highlights the role of horizontal gene transfer from prey species in choanoflagellate genome evolution. Unlike previously studied TEs, the S. rosetta families show evidence for selection on their codon usage, which is shown to act via translational efficiency and translational accuracy.
Mark J. Dayel - One of the best experts on this subject based on the ideXlab platform.
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Prey capture and phagocytosis in the choanoflagellate Salpingoeca rosetta.
PLOS ONE, 2014Co-Authors: Mark J. DayelAbstract:Choanoflagellates are unicellular and colonial aquatic microeukaryotes that capture bacteria using an apical flagellum surrounded by a feeding collar composed of actin-filled microvilli. Flow produced by the apical flagellum drives prey bacteria to the feeding collar for phagocytosis. We report here on the cell biology of prey capture in rosette-shaped colonies and unicellular “thecate” or substrate attached cells from the choanoflagellate S. rosetta. In thecate cells and rosette colonies, phagocytosis initially involves fusion of multiple microvilli, followed by remodeling of the collar membrane to engulf the prey, and transport of engulfed bacteria into the cell. Although both thecate cells and rosette colony cells produce ∼70 nm “collar links” that connect and potentially stabilize adjacent microvilli, only thecate cells were observed to produce a lamellipod-like “collar skirt” that encircles the base of the collar. This study offers insight into the process of prey ingestion by S. rosetta, and provides a context within which to consider potential ecological differences between solitary cells and colonies in choanoflagellates.
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Cooperatively generated stresslet flows supply fresh fluid to multicellular choanoflagellate colonies.
Physical Review Letters, 2013Co-Authors: Marcus Roper, Mark J. Dayel, Rachel E. Pepper, M. A. R. KoehlAbstract:The flagellated protozoan Salpingoeca rosetta is one of the closest relatives of multicellular animals. Unicellular S. rosetta can be induced to form multicellular colonies, but colonies swim more slowly than individual cells so the advantages conferred by colony formation are uncertain. Here we use theoretical models to show that hydrodynamic cooperation between cells can increase the fluid supply to the colony, an important predictor of feeding rate. Our results suggest that hydrodynamic benefits may have been an important selective factor in the evolution of early multicellular animals.
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Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta.
Developmental Biology, 2011Co-Authors: Mark J. Dayel, Tera C. Levin, Rosanna A. Alegado, Scott A. Nichols, Kent L. McdonaldAbstract:It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparisons between animals and their closest living relatives, the choanoflagellates. We report here on the life history, cell differentiation and intercellular interactions in the colony-forming choanoflagellate Salpingoeca rosetta. In response to diverse environmental cues, S. rosetta differentiates into at least five distinct cell types, including three solitary cell types (slow swimmers, fast swimmers, and thecate cells) and two colonial forms (rosettes and chains). Electron microscopy reveals that cells within colonies are held together by a combination of fine intercellular bridges, a shared extracellular matrix, and filopodia. In addition, we have discovered that the carbohydrate-binding protein wheat germ agglutinin specifically stains colonies and the slow swimmers from which they form, showing that molecular differentiation precedes multicellular development. Together, these results help establish S. rosetta as a model system for studying simple multicellularity in choanoflagellates and provide an experimental framework for investigating the origin of animal multicellularity and development.
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Multicellular development in a choanoflagellate
Current Biology, 2010Co-Authors: Mark J. DayelAbstract:Summary Little is known about how the first animals evolved from their single-celled ancestors. Over 120 years ago, Ernst Haeckel proposed that animals evolved through " repeated self-division of [a] primary cell, " [1] an idea supported by the observation that all animals develop from a single cell (the zygote) through successive rounds of cell division [2]. Nonetheless, there are multiple alternative hypotheses [3], including the formal possibility that multicellularity in the progenitor of animals occurred through cell aggregation, with embryogenesis by cell division being secondarily derived. The closest known relatives of animals, choanoflagellates, are emerging as a model system for testing specific hypotheses about animal origins [4–6]. Studying colony formation in choanoflagellates may provide a context for reconstructing the evolution of animal multicellularity. Here, we find that the transition from single cells to multicellular colonies in the choanoflagellate Salpingoeca rosetta (previously known as Proterospongia sp.) occurs by cell division, with sister cells remaining stably attached.
