Accordion waves in Myxococcus xanthus.
Myxococcus xanthus are Gram-negative bacteria that glide on solid surfaces, periodically reversing their direction of movement. When starved, M. xanthus cells organize their movements into waves of cell density that sweep over the colony surface. These waves are unique: Although they appear to interpenetrate, they actually reflect off one another when they collide, so that each wave crest oscillates back and forth with no net displacement. Because the waves reflect the coordinated back and forth oscillations of the individual bacteria, we call them "accordion" waves. The spatial oscillations of individuals are a manifestation of an internal biochemical oscillator, probably involving the Frz chemosensory system. These internal "clocks," each of which is quite variable, are synchronized by collisions between individual cells using a contact-mediated signal-transduction system. The result of collision signaling is that the collective spatial behavior is much less variable than the individual oscillators. In this work, we present experimental observations in which individual cells marked with GFP can be followed in groups of unlabeled cells in monolayer cultures. These data, together with an agent-based computational model demonstrate that the only properties required to explain the ripple patterns are an asymmetric biochemical limit cycle that controls direction reversals and asymmetric contact-induced signaling between cells: Head-to-head signaling is stronger than head-to-tail signaling. Together, the experimental and computational data provide new insights into how populations of interacting oscillators can synchronize and organize spatially to produce morphogenetic patterns that may have parallels in higher organisms.
Sliusarenko
Oleksii
O
Departments of Cell and Molecular Biology and Mathematics, University of California, Berkeley, CA 94720, USA.
Neu
John
J
Zusman
David R
DR
Oster
George
G
D018407:Bacterial Physiological Phenomena; D001426:Bacterial Proteins / Q000502:physiology*; D019521:Body Patterning; D002468:Cell Physiological Phenomena; D002478:Cells, Cultured; D005798:Genes, Bacterial; D049452:Green Fluorescent Proteins / Q000378:metabolism; D007091:Image Processing, Computer-Assisted; D009068:Movement; D016941:Myxococcus xanthus / Q000378:metabolism / Q000502:physiology*; D009991:Oscillometry; D015398:Signal Transduction; D013997:Time Factors
D001426:Bacterial Proteins; D049452:Green Fluorescent Proteins