Publications by year
In Press
(In Press). Abstract.
2021
Williams EA, Jékely G (2021). Nervous systems: Neuropeptides define enigmatic comb-jelly neurons.
Curr Biol,
31(23), R1515-R1517.
Abstract:
Nervous systems: Neuropeptides define enigmatic comb-jelly neurons.
The apparently simple nerve net of comb-jellies has long intrigued biologists. A new study identifies multiple unique neuropeptides in the comb-jelly nervous system and exploits these as indicators of neuronal identity and morphology.
Abstract.
Author URL.
Özpolat BD, Randel N, Williams EA, Bezares-Calderón LA, Andreatta G, Balavoine G, Bertucci PY, Ferrier DEK, Gambi MC, Gazave E, et al (2021). The Nereid on the rise: Platynereis as a model system.
Evodevo,
12(1).
Abstract:
The Nereid on the rise: Platynereis as a model system.
The Nereid Platynereis dumerilii (Audouin and Milne Edwards (Annales des Sciences Naturelles 1:195-269, 1833) is a marine annelid that belongs to the Nereididae, a family of errant polychaete worms. The Nereid shows a pelago-benthic life cycle: as a general characteristic for the superphylum of Lophotrochozoa/Spiralia, it has spirally cleaving embryos developing into swimming trochophore larvae. The larvae then metamorphose into benthic worms living in self-spun tubes on macroalgae. Platynereis is used as a model for genetics, regeneration, reproduction biology, development, evolution, chronobiology, neurobiology, ecology, ecotoxicology, and most recently also for connectomics and single-cell genomics. Research on the Nereid started with studies on eye development and spiralian embryogenesis in the nineteenth and early twentieth centuries. Transitioning into the molecular era, Platynereis research focused on posterior growth and regeneration, neuroendocrinology, circadian and lunar cycles, fertilization, and oocyte maturation. Other work covered segmentation, photoreceptors and other sensory cells, nephridia, and population dynamics. Most recently, the unique advantages of the Nereid young worm for whole-body volume electron microscopy and single-cell sequencing became apparent, enabling the tracing of all neurons in its rope-ladder-like central nervous system, and the construction of multimodal cellular atlases. Here, we provide an overview of current topics and methodologies for P. dumerilii, with the aim of stimulating further interest into our unique model and expanding the active and vibrant Platynereis community.
Abstract.
Author URL.
2020
Hoffmann KH, Williams EA (2020). Editorial: the Evolution of Neuropeptides - a Stroll Through the Animal Kingdom: Updates from the Ottawa 2019 ICCPB Symposium and Beyond. Frontiers in Endocrinology, 11
Williams EA (2020). Function and Distribution of the Wamide Neuropeptide Superfamily in Metazoans. Frontiers in Endocrinology, 11
Gintoli M, Mohanan S, Salter P, Williams E, Beard JD, Jekely G, Corbett AD (2020). Spinning Disk -- Remote Focusing Microscopy.
Abstract:
Spinning Disk -- Remote Focusing Microscopy
Fast confocal imaging was achieved by combining remote focusing with
differential spinning disk optical sectioning to rapidly acquire images of live
samples at cellular resolution. Axial and lateral full width half maxima less
than 5 um and 490 nm respectively are demonstrated over 130 um axial range with
a 256 x 128 um field of view. A water-index calibration slide was used to
achieve an alignment that minimises image volume distortion. Application to
live biological samples was demonstrated by acquiring image volumes over a 24
um axial range at 1 volume/s, allowing for the detection of calcium-based
neuronal activity in Platynereis dumerilii larvae.
Abstract.
Author URL.
Verasztó C, Jasek S, Gühmann M, Shahidi R, Ueda N, Beard JD, Mendes S, Heinz K, Bezares-Calderón LA, Williams E, et al (2020). Whole-animal connectome and cell-type complement of the three-segmented <i>Platynereis dumerilii</i> larva.
Abstract:
Whole-animal connectome and cell-type complement of the three-segmented Platynereis dumerilii larva
AbstractNervous systems coordinate effectors across the body during movements. We know little about the cellular-level structure of synaptic circuits for such body-wide control. Here we describe the whole-body synaptic connectome and cell-type complement of a three-segmented larva of the marine annelid Platynereis dumerilii. We reconstructed and annotated over 1,500 neurons and 6,500 non-neuronal cells in a whole-body serial electron microscopy dataset. The differentiated cells fall into 180 neuronal and 90 non-neuronal cell types. We analyse the modular network architecture of the entire nervous system and describe polysynaptic pathways from 428 sensory neurons to four effector systems – ciliated cells, glands, pigment cells and muscles. The complete somatic musculature and its innervation will be described in a companion paper. We also investigated intersegmental differences in cell-type complement, descending and ascending pathways, and mechanosensory and peptidergic circuits. Our work provides the basis for understanding whole-body coordination in annelids.
Abstract.
2019
Williams EA, Jékely G (2019). Neuronal cell types in the annelid Platynereis dumerilii.
Current Opinion in Neurobiology,
56, 106-116.
Abstract:
Neuronal cell types in the annelid Platynereis dumerilii
The marine annelid Platynereis dumerilii is an invertebrate laboratory model for developmental biology and neuroscience. Its larval stages are small and transparent, enabling whole-body analyses of cell-type diversity and neuronal circuits. Here, we review the diversity of neuronal cell types in Platynereis. A variety of approaches have been used to identify cell types in Platynereis including whole-body gene expression atlases, single-cell RNA-seq and whole-body connectomics through serial EM reconstruction. The function of several cell types and neuronal circuits has also been analysed with experimental approaches. Platynereis has aspects of biology and cell types that are absent from the major invertebrate model organisms (C. elegans and Drosophila) including ciliary locomotion, noradrenergic neurons and ciliary photoreceptor cells.
Abstract.
2018
Williams EA, Carrier T (2018). An -omics Perspective on Marine Invertebrate Larvae. In Carrier T, Heyland A, Reitzel A (Eds.) Evolutionary Ecology of Marine Invertebrate Larvae, Oxford University Press, 288-304.
Schmidt A, Bauknecht P, Williams EA, Augustinowski K, Gründer S, Jékely G (2018). Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis.
Schmidt A, Bauknecht P, Williams EA, Augustinowski K, Gründer S, Jékely G (2018). Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis.
FASEB J,
32(10), 5338-5349.
Abstract:
Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis.
Neuropeptides commonly signal by metabotropic GPCRs. In some mollusks and cnidarians, RFamide neuropeptides mediate fast ionotropic signaling by peptide-gated ion channels that belong to the DEG/ENaC family. Here we describe a neuropeptide system with a dual mode of signaling by both a peptide-gated ion channel and a GPCR. We identified and characterized a peptide-gated channel in the marine annelid Platynereis dumerilii that is specifically activated by Wamide myoinhibitory peptides derived from the same proneuropeptide. The myoinhibitory peptide-gated ion channel (MGIC) belongs to the DEG/ENaC family and is paralogous to RFamide-gated ion channels. Platynereis myoinhibitory peptides also activate a previously described GPCR, MAG. We measured the potency of all Wamides on both MGIC and MAG and identified peptides that preferentially activate one or the other receptor. Analysis of a single-cell transcriptome resource indicates that MGIC and MAG signal in distinct target neurons. The identification of a Wamide-gated ion channel suggests that peptide-gated channels are more diverse and widespread in animals than previously appreciated. The possibility of neuropeptide signaling by both ionotropic and metabotropic receptors to different target cells in the same organism highlights an additional level of complexity in peptidergic signaling networks.-Schmidt, A. Bauknecht, P. Williams, E. A. Augustinowski, K. Gründer, S. Jékely, G. Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis.
Abstract.
Author URL.
Varoqueaux F, Williams EA, Grandemange S, Truscello L, Kamm K, Schierwater B, Jékely G, Fasshauer D (2018). High Cell Diversity and Complex Peptidergic Signaling Underlie Placozoan Behavior.
Curr Biol,
28(21), 3495-3501.e2.
Abstract:
High Cell Diversity and Complex Peptidergic Signaling Underlie Placozoan Behavior.
Placozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioral control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive cells for communication during the rise of animals are not yet understood [1-5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple body plan [6-9]: a thin upper epithelium and a columnar lower epithelium interspersed with a loose layer of fiber cells in between. Its genome contains genes encoding several neuropeptide-precursor-like proteins and orthologs of proteins involved in neurosecretion in animals with a nervous system [10-12]. Here we investigate peptidergic signaling in T. adhaerens. We found specific expression of several neuropeptide-like molecules in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of T. adhaerens. Using live imaging, we discovered that treatments with 11 different peptides elicited striking and consistent effects on the animals' shape, patterns of movement, and velocity that we categorized under three main types: (1) crinkling, (2) turning, and (3) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signaling in nerveless placozoans and suggest that peptidergic volume signaling may have pre-dated synaptic signaling in the evolution of nervous systems.
Abstract.
Author URL.
Varoqueaux F, Williams EA, Grandemange S, Truscello L, Kamm K, Schierwater B, Jékely G, Fasshauer D (2018). High cell diversity and complex peptidergic signalling underlie placozoan behaviour.
Abstract:
High cell diversity and complex peptidergic signalling underlie placozoan behaviour
SUMMARYPlacozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioural control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive communication cells during the rise of animals is not yet understood [1–5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple bodyplan [6–9]: a flat upper epithelium and a cylindrical lower epithelium interspersed with a loose layer of fiber cells. Its genome encodes several proneuropeptide genes and genes involved in neurosecretion in animals with a nervous system [10–12]. Here we investigate neuropeptide signalling in Trichoplax adhaerens. We found specific expression of several neuropeptides in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of Trichoplax adhaerens. Using live imaging, we uncovered that treatments with 11 different neuropeptides elicited striking and consistent effects on the animals’ shape, patterns of movement and velocity that we categorized under three main types: (i) crinkling, (ii) turning, and (iii) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signalling in nerveless placozoans and suggest that peptidergic volume signalling may have predated synaptic signalling in the evolution of nervous systems.
Abstract.
2017
Verasztó C, Ueda N, Bezares-Calderón LA, Panzera A, Williams EA, Shahidi R, Jékely G (2017). Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva.
Elife,
6Abstract:
Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva.
Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.
Abstract.
Author URL.
Verasztó C, Ueda N, Bezares-Calderón LA, Panzera A, Williams EA, Shahidi R, Jékely G (2017). Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the<i>Platynereis</i>larva.
Abstract:
Ciliomotor circuitry underlying whole-body coordination of ciliary activity in thePlatynereislarva
AbstractCiliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae ofPlatynereis dumerilii, a marine annelid.Platynereislarvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.
Abstract.
Williams EA, Verasztó C, Jasek S, Conzelmann M, Shahidi R, Bauknecht P, Mirabeau O, Jékely G (2017). Synaptic and peptidergic connectome of a neurosecretory center in the annelid brain.
Elife,
6Abstract:
Synaptic and peptidergic connectome of a neurosecretory center in the annelid brain.
Neurosecretory centers in animal brains use peptidergic signaling to influence physiology and behavior. Understanding neurosecretory center function requires mapping cell types, synapses, and peptidergic networks. Here we use transmission electron microscopy and gene expression mapping to analyze the synaptic and peptidergic connectome of an entire neurosecretory center. We reconstructed 78 neurosecretory neurons and mapped their synaptic connectivity in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory center expressing many neuropeptides, including hypothalamic peptide orthologs and their receptors. Analysis of peptide-receptor pairs in spatially mapped single-cell transcriptome data revealed sparsely connected networks linking specific neuronal subsets. We experimentally analyzed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signaling. Our study uncovered extensive networks of peptidergic signaling within a neurosecretory center and its connection to the synaptic brain.
Abstract.
Author URL.
Williams EA, Verasztó C, Jasek S, Conzelmann M, Shahidi R, Bauknecht P, Jékely G (2017). Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain.
Abstract:
Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain
AbstractNeurosecretory centres in animal brains use peptidergic signalling to influence physiology and behaviour. Understanding neurosecretory centre function requires mapping cell types, synapses, and peptidergic networks. Here we use electron microscopy and gene expression mapping to analyse the synaptic and peptidergic connectome of an entire neurosecretory centre. We mapped 78 neurosecretory neurons in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory organ expressing many neuropeptides, including hypothalamic peptide orthologues and their receptors. Analysis of peptide-receptor pairs revealed sparsely connected networks linking specific neuronal subsets. We experimentally analysed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signalling. Our study uncovered extensive non-synaptic signalling within a neurosecretory centre and its connection to the synaptic brain.
Abstract.
2016
Williams EA, Jékely G (2016). Towards a systems-level understanding of development in the marine annelid Platynereis dumerilii.
Curr Opin Genet Dev,
39, 175-181.
Abstract:
Towards a systems-level understanding of development in the marine annelid Platynereis dumerilii.
Platynereis dumerilii is a segmented marine worm from the phylum Annelida, a member of the Lophotrochozoans. Platynereis is easily maintained in the lab and exhibits a highly stereotypic development through spiral cleavage with a small, transparent, free-swimming larva highly suitable for microscopy studies. A protocol for embryo microinjection in Platynereis has enabled several genetic tools to be developed, paving the way for functional studies. Recent Platynereis studies have provided insights into the function of several signaling pathways in development. Platynereis has also proven a useful model system for comparative evolutionary developmental studies, allowing the formation of new hypotheses on the evolution of neuroendocrine signaling, body patterning, and organ development. Combining existing large datasets of spatial gene expression mapping, cell lineage mapping, and neuronal circuits with functional analyses of developmental genes represents a promising approach for future studies aiming at a systems-level understanding of development in Platynereis.
Abstract.
Author URL.
2015
Shahidi R, Williams EA, Conzelmann M, Asadulina A, Verasztó C, Jasek S, Bezares-Calderón LA, Jékely G (2015). A serial multiplex immunogold labeling method for identifying peptidergic neurons in connectomes.
Elife,
4Abstract:
A serial multiplex immunogold labeling method for identifying peptidergic neurons in connectomes.
Electron microscopy-based connectomics aims to comprehensively map synaptic connections in neural tissue. However, current approaches are limited in their capacity to directly assign molecular identities to neurons. Here, we use serial multiplex immunogold labeling (siGOLD) and serial-section transmission electron microscopy (ssTEM) to identify multiple peptidergic neurons in a connectome. The high immunogenicity of neuropeptides and their broad distribution along axons, allowed us to identify distinct neurons by immunolabeling small subsets of sections within larger series. We demonstrate the scalability of siGOLD by using 11 neuropeptide antibodies on a full-body larval ssTEM dataset of the annelid Platynereis. We also reconstruct a peptidergic circuitry comprising the sensory nuchal organs, found by siGOLD to express pigment-dispersing factor, a circadian neuropeptide. Our approach enables the direct overlaying of chemical neuromodulatory maps onto synaptic connectomic maps in the study of nervous systems.
Abstract.
Author URL.
Williams EA, Conzelmann M, Jékely G (2015). Myoinhibitory peptide regulates feeding in the marine annelid Platynereis.
Front Zool,
12(1).
Abstract:
Myoinhibitory peptide regulates feeding in the marine annelid Platynereis.
BACKGROUND: During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. How larvae regulate changes in feeding during this life-cycle transition is not well understood. Neuropeptides are known to regulate several aspects of feeding, such as food search, ingestion and digestion. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. The conserved neuropeptide myoinhibitory peptide (MIP) is a key regulator of larval settlement behavior in Platynereis. Whether MIP also regulates the initiation of feeding, another aspect of the pelagic-to-benthic transition in Platynereis, is currently unknown. RESULTS: Here, we explore the contribution of MIP to the regulation of feeding behavior in settled Platynereis postlarvae. We find that in addition to expression in the brain, MIP is expressed in the gut of developing larvae in sensory neurons that densely innervate the hindgut, the foregut, and the midgut. Activating MIP signaling by synthetic neuropeptide addition causes increased gut peristalsis and more frequent pharynx extensions leading to increased food intake. Conversely, morpholino-mediated knockdown of MIP expression inhibits feeding. In the long-term, treatment of Platynereis postlarvae with synthetic MIP increases growth rate and results in earlier cephalic metamorphosis. CONCLUSIONS: Our results show that MIP activates ingestion and gut peristalsis in Platynereis postlarvae. MIP is expressed in enteroendocrine cells of the digestive system suggesting that following larval settlement, feeding may be initiated by a direct sensory-neurosecretory mechanism. This is similar to the mechanism by which MIP induces larval settlement. The pleiotropic roles of MIP may thus have evolved by redeploying the same signaling mechanism in different aspects of a life-cycle transition.
Abstract.
Author URL.
Asadulina A, Conzelmann M, Williams EA, Panzera A, Jékely G (2015). Object-based representation and analysis of light and electron microscopic volume data using Blender.
BMC Bioinformatics,
16Abstract:
Object-based representation and analysis of light and electron microscopic volume data using Blender.
BACKGROUND: Rapid improvements in light and electron microscopy imaging techniques and the development of 3D anatomical atlases necessitate new approaches for the visualization and analysis of image data. Pixel-based representations of raw light microscopy data suffer from limitations in the number of channels that can be visualized simultaneously. Complex electron microscopic reconstructions from large tissue volumes are also challenging to visualize and analyze. RESULTS: Here we exploit the advanced visualization capabilities and flexibility of the open-source platform Blender to visualize and analyze anatomical atlases. We use light-microscopy-based gene expression atlases and electron microscopy connectome volume data from larval stages of the marine annelid Platynereis dumerilii. We build object-based larval gene expression atlases in Blender and develop tools for annotation and coexpression analysis. We also represent and analyze connectome data including neuronal reconstructions and underlying synaptic connectivity. CONCLUSIONS: We demonstrate the power and flexibility of Blender for visualizing and exploring complex anatomical atlases. The resources we have developed for Platynereis will facilitate data sharing and the standardization of anatomical atlases for this species. The flexibility of Blender, particularly its embedded Python application programming interface, means that our methods can be easily extended to other organisms.
Abstract.
Author URL.
2014
Randel N, Asadulina A, Bezares-Calderón LA, Verasztó C, Williams EA, Conzelmann M, Shahidi R, Jékely G (2014). Neuronal connectome of a sensory-motor circuit for visual navigation.
Elife,
3Abstract:
Neuronal connectome of a sensory-motor circuit for visual navigation.
Animals use spatial differences in environmental light levels for visual navigation; however, how light inputs are translated into coordinated motor outputs remains poorly understood. Here we reconstruct the neuronal connectome of a four-eye visual circuit in the larva of the annelid Platynereis using serial-section transmission electron microscopy. In this 71-neuron circuit, photoreceptors connect via three layers of interneurons to motorneurons, which innervate trunk muscles. By combining eye ablations with behavioral experiments, we show that the circuit compares light on either side of the body and stimulates body bending upon left-right light imbalance during visual phototaxis. We also identified an interneuron motif that enhances sensitivity to different light intensity contrasts. The Platynereis eye circuit has the hallmarks of a visual system, including spatial light detection and contrast modulation, illustrating how image-forming eyes may have evolved via intermediate stages contrasting only a light and a dark field during a simple visual task.
Abstract.
Author URL.
2013
Conzelmann M, Williams EA, Tunaru S, Randel N, Shahidi R, Asadulina A, Berger J, Offermanns S, Jékely G (2013). Conserved MIP receptor-ligand pair regulates Platynereis larval settlement.
Proc Natl Acad Sci U S A,
110(20), 8224-8229.
Abstract:
Conserved MIP receptor-ligand pair regulates Platynereis larval settlement.
Life-cycle transitions connecting larval and juvenile stages in metazoans are orchestrated by neuroendocrine signals including neuropeptides and hormones. In marine invertebrate life cycles, which often consist of planktonic larval and benthic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory-neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not yet understood. Here we show that myoinhibitory peptide (MIP)/allatostatin-B, a pleiotropic neuropeptide widespread among protostomes, regulates larval settlement in the marine annelid Platynereis dumerilii. MIP is expressed in chemosensory-neurosecretory cells in the annelid larval apical organ and signals to its receptor, an orthologue of the Drosophila sex peptide receptor, expressed in neighboring apical organ cells. We demonstrate by morpholino-mediated knockdown that MIP signals via this receptor to trigger settlement. These results reveal a role for a conserved MIP receptor-ligand pair in regulating marine annelid settlement.
Abstract.
Author URL.
Conzelmann M, Williams EA, Krug K, Franz-Wachtel M, Macek B, Jékely G (2013). The neuropeptide complement of the marine annelid Platynereis dumerilii.
BMC Genomics,
14Abstract:
The neuropeptide complement of the marine annelid Platynereis dumerilii.
BACKGROUND: the marine annelid Platynereis dumerilii is emerging as a powerful lophotrochozoan experimental model for evolutionary developmental biology (evo-devo) and neurobiology. Recent studies revealed the presence of conserved neuropeptidergic signaling in Platynereis, including vasotocin/neurophysin, myoinhibitory peptide and opioid peptidergic systems. Despite these advances, comprehensive peptidome resources have yet to be reported. RESULTS: the present work describes the neuropeptidome of Platynereis. We established a large transcriptome resource, consisting of stage-specific next-generation sequencing datasets and 77,419 expressed sequence tags. Using this information and a combination of bioinformatic searches and mass spectrometry analyses, we increased the known proneuropeptide (pNP) complement of Platynereis to 98. Based on sequence homology to metazoan pNPs, Platynereis pNPs were grouped into ancient eumetazoan, bilaterian, protostome, lophotrochozoan, and annelid families, and pNPs only found in Platynereis. Compared to the planarian Schmidtea mediterranea, the only other lophotrochozoan with a large-scale pNP resource, Platynereis has a remarkably full complement of conserved pNPs, with 53 pNPs belonging to ancient eumetazoan or bilaterian families. Our comprehensive search strategy, combined with analyses of sequence conservation, also allowed us to define several novel lophotrochozoan and annelid pNP families. The stage-specific transcriptome datasets also allowed us to map changes in pNP expression throughout the Platynereis life cycle. CONCLUSION: the large repertoire of conserved pNPs in Platynereis highlights the usefulness of annelids in comparative neuroendocrinology. This work establishes a reference dataset for comparative peptidomics in lophotrochozoans and provides the basis for future studies of Platynereis peptidergic signaling.
Abstract.
Author URL.
2011
Stewart P, Williams E, Stewart MJ, Soonklang N, Degnan SM, Cummins SF, Hanna PJ, Sobhon P (2011). Characterization of a GABAA receptor ß subunit in the abalone Haliotis asinina that is upregulated during larval development. Journal of Experimental Marine Biology and Ecology, 410, 53-60.
2010
Williams EA (2010). Genetic and environmental interplay during development: Variation at metamorphosis in a natural population of the tropical abalone, Haliotis asinina (Linnaeus).
2009
WILLIAMS EA, DEGNAN SM (2009). Carry‐over effect of larval settlement cue on postlarval gene expression in the marine gastropod <i>Haliotis asinina</i>.
Molecular Ecology,
18(21), 4434-4449.
Abstract:
Carry‐over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina
AbstractThe drastic shift from pelagic larvae to benthic adult form that occurs during marine invertebrate metamorphosis is often induced by intimate interactions between settling larvae and their benthic environment. Larval experience prior to and during metamorphosis can significantly affect adult fitness, but it is presently unknown whether the exact nature of the inductive cue is an experience that matters, or by what mechanism such carry‐over effects are mediated. Here we test for carry‐over effects of the specific nature of inductive cues on gene expression in metamorphosing postlarvae of the tropical abalone, Haliotis asinina. Postlarvae induced by three different species of coralline algae all successfully undergo metamorphosis, yet the expression profiles of 11 of 17 metamorphosis‐related genes differ according to which species of algae the larvae settled upon. Significantly, several genes continue to be differentially expressed for at least 40 h after removal of the algae from the postlarvae, clearly demonstrating a carry‐over effect of inductive cue on gene expression. We observe a carryover effect in several genes with varying functions and spatial expression patterns, indicating that each algal species impacts global gene expression in a unique manner. These data unexpectedly reveal that transcriptional modulation of metamorphosis‐related genes is contingent upon the precise composition of the benthic microenvironment experienced directly at induction of settlement, and highlight transcription as a mechanism that can mediate between larval and postlarval experiences. For new recruits into an abalone population, metamorphosis clearly does not represent a new transcriptional beginning.
Abstract.
Williams EA, Cummins S, Degnan SM (2009). Settlement specifics: Effective induction of abalone settlement and metamorphosis corresponds to biomolecular composition of natural cues.
Communicative and Integrative Biology,
2(4), 347-349.
Abstract:
Settlement specifics: Effective induction of abalone settlement and metamorphosis corresponds to biomolecular composition of natural cues
Chemical signaling plays a major role in shaping life history processes that drive ecology and evolution in marine systems, notably including habitat selection by marine invertebrate larvae that must settle out of the plankton onto the benthos. 1 for larvae, the identification of appropriate habitats in which to settle and undergo metamorphosis to the adult form relies heavily on the recognition of cues indicative of a favorable environment. By documenting settlement responses of larvae of the tropical abalone, Haliotis asinina, to a range of coralline algae species, we recently highlighted the species-specific nature of this interaction. 2 Here, we demonstrate that this specificity is likely driven by chemical, rather than physical, properties of the algae. Our initial characterization of the surface cell biomarkers from three different algal species shows that inductive cue biomolecular composition correlates with variations in larval settlement response. ©2009 Landes Bioscience.
Abstract.
WILLIAMS EA, DEGNAN BM, GUNTER H, JACKSON DJ, WOODCROFT BJ, DEGNAN SM (2009). Widespread transcriptional changes pre‐empt the critical pelagic–benthic transition in the vetigastropod <i>Haliotis asinina</i>.
Molecular Ecology,
18(5), 1006-1025.
Abstract:
Widespread transcriptional changes pre‐empt the critical pelagic–benthic transition in the vetigastropod Haliotis asinina
AbstractLarval settlement is a vital transition period for marine invertebrates and can have far‐reaching effects on the ecology and evolution of a species. To explore the molecular mechanisms of this critical process in a nonmodel organism, the abalone Haliotis asinina, we employed cDNA microarrays. By comparing gene expression profiles through mid‐ to late larval development and metamorphosis, we identified 144 genes as candidates for a role in competence and/or metamorphosis. Gene characterization indicates ~60% of these are significantly similar to known genes from other taxa, while ~40% are novel. A high 49.3% of genes are gastropod or abalone specific, but none appears to be Lophotrochozoan specific, even though metamorphosis is thought to have had a separate origin in this group. Differentially expressed larval and postlarval genes can be clustered into five categories that reveal strikingly different temporal transcriptional patterns occurring during this phase of development. Some gene activation is contingent upon exogenous cues and correlates with initiation of settlement. Importantly, there is also extensive gene activity associated with the endogenous attainment of competence, which occurs before, and independent of, the exogenous induction of settlement. Our results show that as the haliotid veliger larva matures, it requires coordinated regulation of temporally different batteries of genes involved in a wide range of physiological and developmental processes associated with benthic colonization. Although the signalling pathways operating at metamorphosis may be conserved across the animal kingdom, it appears they regulate the expression of novel genes specific to abalone, gastropods and molluscs during H. asinina metamorphosis.
Abstract.
2008
Williams EA, Craigie A, Yeates A, Degnan SM (2008). Articulated Coralline Algae of the Genus<i>Amphiroa</i>Are Highly Effective Natural Inducers of Settlement in the Tropical Abalone<i>Haliotis asinina</i>. The Biological Bulletin, 215(1), 98-107.
2006
Jacobs MW, Degnan SM, Woods R, Williams E, Roper KE, Green K, Degnan BM (2006). The effect of larval age on morphology and gene expression during ascidian metamorphosis. Integrative and Comparative Biology, 46(6), 760-776.
