Coordination Across Scales — Or Why We Study Organisms

Kloster Schöntal, The 3DMM2O Conference
March 23-27, 2024

Gáspár Jékely

Centre for Organismal Studies, Heidelberg University

@jekely@biologists.social

Platynereis dumerilii







  • breeding culture
  • genome sequence
  • microinjection, transgenesis
  • neuron-specific promoters
  • knock-out lines
  • neuronal connectome
  • neuronal activity imaging

Larval behaviours



phototaxis

  • UV avoidance
  • thermosensing
  • settlement

startle response

  • ciliary coordination
  • chemosensing

crawling

  • flow sensing
  • pressure response

Eukaryotic cilia

Emelie Brodrick


Lin et al, 2018

  • distributed actuation

Multiciliated cells form ciliary bands

Metachronal waves

  • high-speed imaging
  • metachronal waves
  • large-scale coordination of cilia
  • coupled oscillators
  • theory: mediated by hydrodynamic coupling

Precise orientation of multiciliary arrays

expansion microscopy

Precise orientation of multiciliary arrays

expansion microscopy

Volume EM with Array Tomograpy

Array tomography workflow

Array tomography workflow

Array tomography workflow

Whole-body vEM reconstruction

Synaptic connectome

Whole-body annotation of all ciliary basal bodies

Whole-body annotation of all ciliary basal bodies


  • ~10,000 motile cilia
  • high degree of left-right symmetry
  • 3D additive manufacturing from anterior to posterior of the cell

Whole-body annotation of all ciliary basal bodies

Simulation of ciliary flows

with Eric Keaveny, Imperial College

  • mathematical modelling of thousands of cilia
  • simulation of flow fields
  • metachrony maximises flows
  • all mathematical models of metacrony use hydrodynamic coupling

Cilia in each cell beat with different frequencies


  • quantification of ciliary beat frequency for each cell
  • values constant for individual cells
  • discontinuity between cells

Metachronal waves - phase locking only within cells


  • conversion of intensity plot into Hilbert phase, φ(θ, t) (from 0 to 2π over a full beat cycle)
  • strong phase locking within cells (∆φ(t) = φ1(t) − φ2(t) constant over time)
  • no phase locking between cells

Tiny gaps introduced by laser ablation break phase locking


  • pulsed UV laser-ablation of patches of cilia
  • phase locking is lost across the gap, maintained in the continuous patches

No global coordination via flow

  • progressive ablation of most cilia
  • small patch maintains metachrony and phase locking

Ciliary arrests are globally coordinated

  • ciliary arrests occur regularly (~1/min)
  • all cilia close simultaneously

Closures are induced by rise in intracellular calcium







Closures are induced by a single giant motoneuron

Coordination of closures across different bands of cilia

How are different ciliomotor neurons coordinated?

Envoi

  • 3DMM2O: organisms can provide inspiration

  • hierarchical 3D organisation

  • multi-scale coordination

  • extreme reproducibility of shape and function

Acknowledgements

Lab members

  • Sanja Jasek
  • Alexandra Kerbl
  • Emily Savage
  • Simone Wolters
  • Lara Keweloh
  • Kevin Urbansky
  • Karel Mocaer
  • David Hug
  • Benedikt Dürr
  • Ira Maegele
  • Emelie Brodrick (Exeter)

Facilities

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