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Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates.

ABSTRACT: Choanoflagellates, eukaryotes that are important predators on bacteria in aquatic ecosystems, are closely related to animals and are used as a model system to study the evolution of animals from protozoan ancestors. The choanoflagellate Salpingoeca rosetta has a complex life cycle with different morphotypes, some unicellular and some multicellular. Here we use computational fluid dynamics to study the hydrodynamics of swimming and feeding by different unicellular stages of S. rosetta: a swimming cell with a collar of prey-capturing microvilli surrounding a single flagellum, a thecate cell attached to a surface and a dispersal-stage cell with a slender body, long flagellum and short collar. We show that a longer flagellum increases swimming speed, longer microvilli reduce speed and cell shape only affects speed when the collar is very short. The flux of prey-carrying water into the collar capture zone is greater for swimming than sessile cells, but this advantage decreases with collar size. Stalk length has little effect on flux for sessile cells. We show that ignoring the collar, as earlier models have done, overestimates flux and greatly overestimates the benefit to feeding performance of swimming versus being attached, and of a longer stalk for attached cells.

SUBMITTER: Nguyen H

PROVIDER: S-EPMC6364633 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates.

Nguyen Hoa H Koehl M A R MAR Oakes Christian C Bustamante Greg G Fauci Lisa L

Journal of the Royal Society, Interface 20190101 150

Choanoflagellates, eukaryotes that are important predators on bacteria in aquatic ecosystems, are closely related to animals and are used as a model system to study the evolution of animals from protozoan ancestors. The choanoflagellate Salpingoeca rosetta has a complex life cycle with different morphotypes, some unicellular and some multicellular. Here we use computational fluid dynamics to study the hydrodynamics of swimming and feeding by different unicellular stages of S. rosetta: a swimming ...[more]

PMID: 30958167

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Project description:BACKGROUND:Functional inference on the attachment of acanthocephalans has generally been drawn directly from morphology. However, performance of structures is often non-intuitive and context-dependent, thus performance analysis should be included whenever possible to improve functional interpretation. In acanthocephalans, performance analysis of attachment is available only for Acanthocephalus ranae, a species that solely relies on the proboscis to attach. Here we compare body morphology and muscle arrangement in 13 species of Corynosoma, which use their spiny body as a fundamental holdfast. A basic performance analysis using live cystacanths of two representative species is also provided. METHODS:Adults of 13 Corynosoma spp. were obtained from 11 marine mammal species. Specimens were cut and carefully cleaned to examine muscle arrangement through light and scanning electron microscopy. Live cystacanths of C. australe and C. cetaceum were selected for performance analysis. Video records of evagination-invagination cycles of the proboscis were obtained and analysed with a video editor. RESULTS:The basic arrangement of proboscis retractors, trunk circular and longitudinal muscles, neck retractors and receptacle retractors, was conserved in all Corynosoma species. Interspecific variability was found in the relative development of disk muscles: minimum in C. enhydri, maximum in C. cetaceum; the distal insertion of the ventral neck retractor: ventro-lateral in C. cetaceum, C. hamannni and C. pseudohamanni and ventral in the other species; and the distal insertion of the receptacle retractors: more proximal in species with a longer hindtrunk. Performance analysis indicated striking similarities to that described for A. ranae except that (i) the foretrunk bends ventrally during the evagination-invagination cycles of the proboscis; (ii) disk muscles can flatten the tip of the foretrunk regardless of these cycles; and (iii) the receptacle bends ventrally and is driven to the hindtrunk by coordinated action of receptacle retractors. CONCLUSIONS:Species of Corynosoma are able to use up to six holfast mechanisms. Attachment relies on a similar performance to that described for A. ranae. However, structural ventral bending of an inflated, spiny foretrunk, with a parallel re-arrangement of foretrunk muscles, have generated unexpected novel functions that make attachment extremely effective in species of Corynosoma. Interspecific variability in trunk shape and muscle arrangement grossly correlates with the rheological conditions each species experiences in their microhabitats within the gut of marine mammals.

Project description:BackgroundComparative genomics of the early diverging metazoan lineages and of their unicellular sister-groups opens new window to reconstructing the genetic changes which preceded or accompanied the evolution of multicellular body plans. A recent analysis found that the genome of the nerve-less sponges encodes the homologues of most vertebrate post-synaptic proteins. In vertebrate excitatory synapses, these proteins assemble to form the post-synaptic density, a complex molecular platform linking membrane receptors, components of their signalling pathways, and the cytoskeleton. Newly available genomes from Monosiga brevicollis (a member of Choanoflagellata, the closest unicellular relatives of animals) and Trichoplax adhaerens (a member of Placozoa: besides sponges, the only nerve-less metazoans) offer an opportunity to refine our understanding of post-synaptic protein evolution.ResultsSearches for orthologous proteins and reconstruction of gene gains/losses based on the taxon phylogeny indicate that post-synaptic proteins originated in two main steps. The backbone scaffold proteins (Shank, Homer, DLG) and some of their partners were acquired in a unicellular ancestor of choanoflagellates and metazoans. A substantial additional set appeared in an exclusive ancestor of the Metazoa. The placozoan genome contains most post-synaptic genes but lacks some of them. Notably, the master-scaffold protein Shank might have been lost secondarily in the placozoan lineage.ConclusionsThe time of origination of most post-synaptic proteins was not concomitant with the acquisition of synapses or neural-like cells. The backbone of the scaffold emerged in a unicellular context and was probably not involved in cell-cell communication. Based on the reconstructed protein composition and potential interactions, its ancestral function could have been to link calcium signalling and cytoskeleton regulation. The complex later became integrated into the evolving synapse through the addition of novel functionalities.

Project description:Simple Summary Herbivorous insects and plants greatly affected each other’s evolution due to their close interactions. This resulted in the development of a variety of adaptations on both sides. Through the need for protection against herbivorous insects, surfaces with lower attachment ability evolved in many plants. As a response, the attachment systems of insects have developed numerous specializations. Stick insects (Phasmatodea) have an attachment system, consisting of paired claws, arolium (attachment pad between the claws) and euplantulae (paired attachment pads on the tarsomeres), which is well adapted to different natural surfaces. We used measurements of pull-off and traction force in two species (Medauroidea extradentata and Sungaya inexpectata) representing the most common microstructures used for attachment within stick insects (nubby and smooth) to quantify the attachment ability of Phasmatodea on natural surfaces. Plant leaves with different surface properties (smooth, trichome-covered, hydrophilic and covered with crystalline waxes) were selected as substrates. Wax-crystal-covered fine-roughness substrates revealed the lowest, whereas strongly structured substrates showed the highest attachment performance among the stick insects studied. Removing the claws of the insects resulted in lower attachment ability on structured substrates. Furthermore, claw removal revealed that the attachment performance of the pads is less reduced by contaminating wax crystals in the species with nubby attachment structures. Long-lasting effects of the leaves on the attachment ability were briefly investigated, but not confirmed. Abstract Herbivorous insects and plants exemplify a longstanding antagonistic coevolution, resulting in the development of a variety of adaptations on both sides. Some plant surfaces evolved features that negatively influence the performance of the attachment systems of insects, which adapted accordingly as a response. Stick insects (Phasmatodea) have a well-adapted attachment system with paired claws, pretarsal arolium and tarsal euplantulae. We measured the attachment ability of Medauroidea extradentata with smooth surface on the euplantulae and Sungaya inexpectata with nubby microstructures of the euplantulae on different plant substrates, and their pull-off and traction forces were determined. These species represent the two most common euplantulae microstructures, which are also the main difference between their respective attachment systems. The measurements were performed on selected plant leaves with different properties (smooth, trichome-covered, hydrophilic and covered with crystalline waxes) representing different types among the high diversity of plant surfaces. Wax-crystal-covered substrates with fine roughness revealed the lowest, whereas strongly structured substrates showed the highest attachment ability of the Phasmatodea species studied. Removal of the claws caused lower attachment due to loss of mechanical interlocking. Interestingly, the two species showed significant differences without claws on wax-crystal-covered leaves, where the individuals with nubby euplantulae revealed stronger attachment. Long-lasting effects of the leaves on the attachment ability were briefly investigated, but not confirmed.

Dataset Information

Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates.

Publications

Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates.

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