Multimodal ciliary photoreceptors for UV and pressure sensing in marine zooplankton

University of Sussex
April 24, 2025

Gáspár Jékely

Centre for Organismal Studies, Heidelberg University

@jekely@biologists.social

Responses of marine animals to changes in pressure

Platynereis dumerilii







  • breeding culture, full life-cycle
  • embryos daily, year round
  • genome sequence
  • microinjection, transgenesis
  • neuron-specific promoters and antibodies
  • knock-out lines
  • neuronal connectome
  • whole-body neuronal activity imaging
  • whole-animal pharmacology by bath application 😎

Platynereis dumerilii















Spawning
movie by Albrecht Fischer


Synchronously developing larvae

Pressure response in Platynereis larvae

Precise control of pressure in the pressure chamber

Pressure response is graded

Swimming speed increases, trajectories straighten

ctr

pressure

Ciliary beating increases under pressure



Which cells respond to pressure?

Microscopy pressure chamber

Calcium imaging

Pressure is sensed by photoreceptors with ramified cilia

Photoreceptor responses to pressure are graded


Defects of pressure response in c-opsin1 mutants

Reduced ciliary compartment in c-opsin1 mutants



Defects of ciliary ultrastructure in c-opsin1 mutants



Whole-body volume EM of an entire three-day-old larva


Synaptic connectome

Synaptic connectome

Head neuropils and connectivity

Circuitry of ciliary photoreceptors


Serotonergic neurons to activate cilia

Ser-h1 neurons, EM reconstruction

Pressure increases ciliary beating through serotonergic cells

Mechanism of barotaxis

UV response in Platynereis larvae

UV avoidance is dependent on c-opsin1

How can cPRCs mediate two responses with opposing sign?



c-opsin1-dependent UV response



Strong cPRC activation after UV exposure

Nitric-oxide synthase in postsynaptic interneurons

      HCR             Transgenic labelling         immunostaining

NO is produced in the neuropil after UV stimulation

NOS mutants have altered cPRC response

NOS mutants have altered INRGW and motoneuron response

NOS mutants show defective UV avoidance

Two unusual guanylyl cyclases in the cPRCs

NIT-GC1 RNA
NIT-GC1 protein
NIT-GC2 RNA
NIT-GC2 protein

Two unusual guanylyl cyclases in the cPRCs

NIT-GC1 mediates NO-feedback

NIT-GC2 mediates phototransduction

Mathematical modelling of the circuit

Model fitting

wild type
NOS-11
NOS-23
NIT-GC2 mo.

Integration and memory of UV exposure

Up or down?

‘front-wheel drive’ head cilia fast

‘rear-wheel drive’ head cilia slow

but reviewer 2 asked us to …


ciliary beat frequency


Swimming speed

Acknowledgements

  • Alexandra Kerbl
  • Karel Mocaer
  • Sanja Jasek
  • David Hug
  • Jules Duruz
  • Mateusz Kostecki
  • Benedikt Dürr
  • Kata Szabó
  • Iva Verbanac
  • Lara Keweloh
  • Emily Savage
  • Simone Wolters
  • Selin Heinzelmann
  • Kevin Urbansky

Alumni

  • Kei Jokura (NIBB, Okazaki)
  • Luis Bezares (LBDV, Villefranche-sur-mer)
  • Emelie Brodrick (Sussex)

Facilities

  • EM Core Facility
    • Réza Shahidi
    • Charlotta Funaya
  • Nikon Imaging Centre
    • Ulrike Engel