Vicky Sleight
@abdn.ac.uk
Lecturer, School of Biological Sciences
University of Aberdeen
RESEARCH, TEACHING, or OTHER INTERESTS
Developmental Biology, Animal Science and Zoology, Ecology, Evolution, Behavior and Systematics, Embryology
Scopus Publications
Scopus Publications
Victoria A Sleight
Oxford University Press (OUP)
Abstract Biomineralisation is the process by which living organisms produce hard structures such as shells and bone. There are multiple independent origins of biomineralised skeletons across the tree of life. This review gives a glimpse into the diversity of spiralian biominerals and what they can teach us about the evolution of novelty. It discusses different levels of biological organisation that may be informative to understand the evolution of biomineralisation and considers the relationship between skeletal and non-skeletal biominerals. More specifically, this review explores if cell type and gene regulatory network approaches could enhance our understanding of the evolutionary origins of biomineralisation.
Ferdinand Marlétaz, Elisa de la Calle-Mustienes, Rafael D. Acemel, Christina Paliou, Silvia Naranjo, Pedro Manuel Martínez-García, Ildefonso Cases, Victoria A. Sleight, Christine Hirschberger, Marina Marcet-Houben,et al.
Springer Science and Business Media LLC
AbstractSkates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments1,2. However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.
Jenaid M Rees, Victoria A Sleight, Stephen J Clark, Tetsuya Nakamura, and J Andrew Gillis
eLife Sciences Publications, Ltd
The gill skeleton of cartilaginous fishes (sharks, skates, rays, and holocephalans) exhibits a striking anterior–posterior polarity, with a series of fine appendages called branchial rays projecting from the posterior margin of the gill arch cartilages. We previously demonstrated in the skate (Leucoraja erinacea) that branchial rays derive from a posterior domain of pharyngeal arch mesenchyme that is responsive to Sonic hedgehog (Shh) signaling from a distal gill arch epithelial ridge (GAER) signaling centre. However, how branchial ray progenitors are specified exclusively within posterior gill arch mesenchyme is not known. Here, we show that genes encoding several Wnt ligands are expressed in the ectoderm immediately adjacent to the skate GAER, and that these Wnt signals are transduced largely in the anterior arch environment. Using pharmacological manipulation, we show that inhibition of Wnt signalling results in an anterior expansion of Shh signal transduction in developing skate gill arches, and in the formation of ectopic anterior branchial ray cartilages. Our findings demonstrate that ectodermal Wnt signalling contributes to gill arch skeletal polarity in skate by restricting Shh signal transduction and chondrogenesis to the posterior arch environment and highlights the importance of signalling interactions at embryonic tissue boundaries for cell fate determination in vertebrate pharyngeal arches.
Alessandro Cavallo, Melody S. Clark, Lloyd S. Peck, Elizabeth M. Harper, and Victoria A. Sleight
The Royal Society
Adult molluscs produce shells with diverse morphologies and ornamentations, different colour patterns and microstructures. The larval shell, however, is a phenotypically more conserved structure. How do developmental and evolutionary processes generate varying diversity at different life-history stages within a species? Using live imaging, histology, scanning electron microscopy and transcriptomic profiling, we have described shell development in a heteroconchian bivalve, the Antarctic clam, Laternula elliptica, and compared it to adult shell secretion processes in the same species . Adult downstream shell genes, such as those encoding extracellular matrix proteins and biomineralization enzymes, were largely not expressed during shell development. Instead, a development-specific downstream gene repertoire was expressed. Upstream regulatory genes such as transcription factors and signalling molecules were largely conserved between developmental and adult shell secretion. Comparing heteroconchian data with recently reported pteriomorphian larval shell development data suggests that, despite being phenotypically more conserved, the downstream effectors constituting the larval shell ‘tool-kit’ may be as diverse as that of adults. Overall, our new data suggest that a larval shell formed using development-specific downstream effector genes is a conserved and ancestral feature of the bivalve lineage, and possibly more broadly across the molluscs.
J. Andrew Gillis, Scott Bennett, Katharine E. Criswell, Jenaid Rees, Victoria A. Sleight, Christine Hirschberger, Dan Calzarette, Sarah Kerr, and Jeremy Dasen
Elsevier
Helena García-Castro, Nathan J. Kenny, Marta Iglesias, Patricia Álvarez-Campos, Vincent Mason, Anamaria Elek, Anna Schönauer, Victoria A. Sleight, Jakke Neiro, Aziz Aboobaker,et al.
Springer Science and Business Media LLC
AbstractSingle-cell sequencing technologies are revolutionizing biology, but they are limited by the need to dissociate live samples. Here, we present ACME (ACetic-MEthanol), a dissociation approach for single-cell transcriptomics that simultaneously fixes cells. ACME-dissociated cells have high RNA integrity, can be cryopreserved multiple times, and are sortable and permeable. As a proof of principle, we provide single-cell transcriptomic data of different species, using both droplet-based and combinatorial barcoding single-cell methods. ACME uses affordable reagents, can be done in most laboratories and even in the field, and thus will accelerate our knowledge of cell types across the tree of life.
Christine Hirschberger, Victoria A Sleight, Katharine E Criswell, Stephen J Clark, and J Andrew Gillis
Oxford University Press (OUP)
AbstractThe origin of the jaw is a long-standing problem in vertebrate evolutionary biology. Classical hypotheses of serial homology propose that the upper and lower jaw evolved through modifications of dorsal and ventral gill arch skeletal elements, respectively. If the jaw and gill arches are derived members of a primitive branchial series, we predict that they would share common developmental patterning mechanisms. Using candidate and RNAseq/differential gene expression analyses, we find broad conservation of dorsoventral (DV) patterning mechanisms within the developing mandibular, hyoid, and gill arches of a cartilaginous fish, the skate (Leucoraja erinacea). Shared features include expression of genes encoding members of the ventralizing BMP and endothelin signaling pathways and their effectors, the joint markers nkx3.2 and gdf5 and prochondrogenic transcription factor barx1, and the dorsal territory marker pou3f3. Additionally, we find that mesenchymal expression of eya1/six1 is an ancestral feature of the mandibular arch of jawed vertebrates, whereas differences in notch signaling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the DV axis of the pharyngeal arches, including scamp5 as a novel marker of the dorsal mandibular arch, as well as distinct transcriptional features of mandibular and gill arch muscle progenitors and developing gill buds. Taken together, our findings reveal conserved patterning mechanisms in the pharyngeal arches of jawed vertebrates, consistent with serial homology of their skeletal derivatives, as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies.
Melody S. Clark, Lloyd S. Peck, Jaison Arivalagan, Thierry Backeljau, Sophie Berland, Joao C. R. Cardoso, Carlos Caurcel, Gauthier Chapelle, Michele De Noia, Sam Dupont,et al.
Wiley
Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO3 crystals form complex biocomposites with proteins, which although typically less than 5% of total shell mass, play significant roles in determining shell microstructure. Despite much research effort, large knowledge gaps remain in how molluscs construct and maintain their shells, and how they produce such a great diversity of forms. Here we synthesize results on how shell shape, microstructure, composition and organic content vary among, and within, species in response to numerous biotic and abiotic factors. At the local level, temperature, food supply and predation cues significantly affect shell morphology, whilst salinity has a much stronger influence across latitudes. Moreover, we emphasize how advances in genomic technologies [e.g. restriction site‐associated DNA sequencing (RAD‐Seq) and epigenetics] allow detailed examinations of whether morphological changes result from phenotypic plasticity or genetic adaptation, or a combination of these. RAD‐Seq has already identified single nucleotide polymorphisms associated with temperature and aquaculture practices, whilst epigenetic processes have been shown significantly to modify shell construction to local conditions in, for example, Antarctica and New Zealand. We also synthesize results on the costs of shell construction and explore how these affect energetic trade‐offs in animal metabolism. The cellular costs are still debated, with CaCO3 precipitation estimates ranging from 1–2 J/mg to 17–55 J/mg depending on experimental and environmental conditions. However, organic components are more expensive (~29 J/mg) and recent data indicate transmembrane calcium ion transporters can involve considerable costs. This review emphasizes the role that molecular analyses have played in demonstrating multiple evolutionary origins of biomineralization genes. Although these are characterized by lineage‐specific proteins and unique combinations of co‐opted genes, a small set of protein domains have been identified as a conserved biomineralization tool box. We further highlight the use of sequence data sets in providing candidate genes for in situ localization and protein function studies. The former has elucidated gene expression modularity in mantle tissue, improving understanding of the diversity of shell morphology synthesis. RNA interference (RNAi) and clustered regularly interspersed short palindromic repeats ‐ CRISPR‐associated protein 9 (CRISPR‐Cas9) experiments have provided proof of concept for use in the functional investigation of mollusc gene sequences, showing for example that Pif (aragonite‐binding) protein plays a significant role in structured nacre crystal growth and that the Lsdia1 gene sets shell chirality in Lymnaea stagnalis. Much research has focused on the impacts of ocean acidification on molluscs. Initial studies were predominantly pessimistic for future molluscan biodiversity. However, more sophisticated experiments incorporating selective breeding and multiple generations are identifying subtle effects and that variability within mollusc genomes has potential for adaption to future conditions. Furthermore, we highlight recent historical studies based on museum collections that demonstrate a greater resilience of molluscs to climate change compared with experimental data. The future of mollusc research lies not solely with ecological investigations into biodiversity, and this review synthesizes knowledge across disciplines to understand biomineralization. It spans research ranging from evolution and development, through predictions of biodiversity prospects and future‐proofing of aquaculture to identifying new biomimetic opportunities and societal benefits from recycling shell products.
Abigail Ramsøe, Melody S. Clark, and Victoria A. Sleight
Springer Science and Business Media LLC
AbstractA computationally predicted gene regulatory network (GRN), generated from mantle-specific gene expression profiles in the Antarctic clam Laternula elliptica, was interrogated to test the regulation and interaction of duplicated inducible hsp70 paralogues. hsp70A and hsp70B were identified in the GRN with each paralogue falling into unique submodules that were linked together by a single shared second neighbour. Annotations associated with the clusters in each submodule suggested that hsp70A primarily shares regulatory relationships with genes encoding ribosomal proteins, where it may have a role in protecting the ribosome under stress. hsp70B, on the other hand, interacted with a suite of genes involved in signalling pathways, including four transcription factors, cellular response to stress and the cytoskeleton. Given the contrasting submodules and associated annotations of the two hsp70 paralogues, the GRN analysis suggests that each gene is carrying out additional separate functions, as well as being involved in the traditional chaperone heat stress response, and therefore supports the hypothesis that subfunctionalization has occurred after gene duplication. The GRN was specifically produced from experiments investigating biomineralization; however, this study shows the utility of such data for investigating multiple questions concerning gene duplications, interactions and putative functions in a non-model species.
Victoria A Sleight and J Andrew Gillis
eLife Sciences Publications, Ltd
Paired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.
Victoria A Sleight, Philipp Antczak, Francesco Falciani, and Melody S Clark
Oxford University Press (OUP)
Abstract Motivation The molecular processes regulating molluscan shell production remain relatively uncharacterized, despite the clear evolutionary and societal importance of biomineralization. Results Here we built the first computationally predicted gene regulatory network (GRN) for molluscan biomineralization using Antarctic clam (Laternula elliptica) mantle gene expression data produced over an age-categorized shell damage-repair time-course. We used previously published in vivo in situ hybridization expression data to ground truth gene interactions predicted by the GRN and show that candidate biomineralization genes from different shell layers, and hence microstructures, were connected in unique modules. We characterized two biomineralization modules of the GRN and hypothesize that one module is responsible for translating the extracellular proteins required for growing, repairing or remodelling the nacreous shell layer, whereas the second module orchestrates the transport of both ions and proteins to the shell secretion site, which are required during normal shell growth, and repair. Our findings demonstrate that unbiased computational methods are particularly valuable for studying fundamental biological processes and gene interactions in non-model species where rich sources of gene expression data exist, but annotation rates are poor and the ability to carry out true functional tests are still lacking. Availability and implementation The raw RNA-Seq data is freely available for download from NCBI SRA (Accession: PRJNA398984), the assembled and annotated transcriptome can be viewed and downloaded from molluscDB (ensembl.molluscdb.org) and in addition, the assembled transcripts, reconstructed GRN, modules and detailed annotations are all available as Supplementary Files. Supplementary information Supplementary data are available at Bioinformatics online.
Victoria A. Sleight, Lloyd S. Peck, Elisabeth A. Dyrynda, Valerie J. Smith, and Melody S. Clark
Springer Science and Business Media LLC
P Sleight, V Sleight, A Dawson, and N Januszewski
BMJ
Peter Joseph Wilkinson Monks was born in Warrington, Cheshire, and studied medicine at St Bartholomew’s Hospital, London. His preclinical training was relocated to Cambridge during the war. He was a medical student and junior doctor during the second world war, treating casualties of the London Blitz and experiencing direct bombing of the hospital itself. After the war, in the Royal Naval Volunteer Reserve, he met and married Phyl (Phyllis), a young officer in the WRNS.
His initial appointment was as surgeon lieutenant at Greenwich Hospital, and …
Victoria A. Sleight, Adil Bakir, Richard C. Thompson, and Theodore B. Henry
Elsevier BV
Jaison Arivalagan, Tejaswi Yarra, Benjamin Marie, Victoria A. Sleight, Evelyne Duvernois-Berthet, Melody S. Clark, Arul Marie, and Sophie Berland
Oxford University Press (OUP)
Bivalves have evolved a range of complex shell forming mechanisms that are reflected by their incredible diversity in shell mineralogy and microstructures. A suite of proteins exported to the shell matrix space plays a significant role in controlling these features, in addition to underpinning some of the physical properties of the shell itself. Although, there is a general consensus that a minimum basic protein tool kit is required for shell construction, to date, this remains undefined. In this study, the shell matrix proteins (SMPs) of four highly divergent bivalves (The Pacific oyster, Crassostrea gigas; the blue mussel, Mytilus edulis; the clam, Mya truncata, and the king scallop, Pecten maximus) were analyzed in an identical fashion using proteomics pipeline. This enabled us to identify the critical elements of a “basic tool kit” for calcification processes, which were conserved across the taxa irrespective of the shell morphology and arrangement of the crystal surfaces. In addition, protein domains controlling the crystal layers specific to aragonite and calcite were also identified. Intriguingly, a significant number of the identified SMPs contained domains related to immune functions. These were often are unique to each species implying their involvement not only in immunity, but also environmental adaptation. This suggests that the SMPs are selectively exported in a complex mix to endow the shell with both mechanical protection and biochemical defense.
Victoria A. Sleight, Benjamin Marie, Daniel J. Jackson, Elisabeth A. Dyrynda, Arul Marie, and Melody S. Clark
Springer Science and Business Media LLC
AbstractThe Antarctic clam Laternula elliptica lives almost permanently below 0 °C and therefore is a valuable and tractable model to study the mechanisms of biomineralisation in cold water. The present study employed a multidisciplinary approach using histology, immunohistochemistry, electron microscopy, proteomics and gene expression to investigate this process. Thirty seven proteins were identified via proteomic extraction of the nacreous shell layer, including two not previously found in nacre; a novel T-rich Mucin-like protein and a Zinc-dependent metalloprotease. In situ hybridisation of seven candidate biomineralisation genes revealed discrete spatial expression patterns within the mantle tissue, hinting at modular organisation, which is also observed in the mantle tissues of other molluscs. All seven of these biomineralisation candidates displayed evidence of multifunctionality and strong association with vesicles, which are potentially involved in shell secretion in this species.
Jaison Arivalagan, Benjamin Marie, Victoria A. Sleight, Melody S. Clark, Sophie Berland, and Arul Marie
Elsevier BV
Victoria A. Sleight, Michael A.S. Thorne, Lloyd S. Peck, Jaison Arivalagan, Sophie Berland, Arul Marie, and Melody S. Clark
Elsevier BV
Victoria A. Sleight, Michael A.S. Thorne, Lloyd S. Peck, and Melody S. Clark
Elsevier BV
Lucy C. Woodall, Anna Sanchez-Vidal, Miquel Canals, Gordon L.J. Paterson, Rachel Coppock, Victoria Sleight, Antonio Calafat, Alex D. Rogers, Bhavani E. Narayanaswamy, and Richard C. Thompson
The Royal Society
Marine debris, mostly consisting of plastic, is a global problem, negatively impacting wildlife, tourism and shipping. However, despite the durability of plastic, and the exponential increase in its production, monitoring data show limited evidence of concomitant increasing concentrations in marine habitats. There appears to be a considerable proportion of the manufactured plastic that is unaccounted for in surveys tracking the fate of environmental plastics. Even the discovery of widespread accumulation of microscopic fragments (microplastics) in oceanic gyres and shallow water sediments is unable to explain the missing fraction. Here, we show that deep-sea sediments are a likely sink for microplastics. Microplastic, in the form of fibres, was up to four orders of magnitude more abundant (per unit volume) in deep-sea sediments from the Atlantic Ocean, Mediterranean Sea and Indian Ocean than in contaminated sea-surface waters. Our results show evidence for a large and hitherto unknown repository of microplastics. The dominance of microfibres points to a previously underreported and unsampled plastic fraction. Given the vastness of the deep sea and the prevalence of microplastics at all sites we investigated, the deep-sea floor appears to provide an answer to the question— where is all the plastic?