Biological soliton in multicellular movement

Abstract

Solitons have been observed in various physical phenomena. Here, we show that the distinct characteristics of solitons are present in the mass cell movement of non-chemotactic mutants of the cellular slime mould Dictyostelium discoideum. During starvation, D. discoideum forms multicellular structures that differentiate into spore or stalk cells and, eventually, a fruiting body. Non-chemotactic mutant cells do not form multicellular structures; however, they do undergo mass cell movement in the form of a pulsatile soliton-like structure (SLS). We also found that SLS induction is mediated by adhesive cell-cell interactions. These observations provide novel insights into the mechanisms of biological solitons in multicellular movement.

Figure 1. Multicellular movement of the non-chemotactic D. discoideum KI-5 mutant shows soliton-like structures (SLSs) which behave similarly to soliton waves.

(a, b), Formation of multicellular structures in parental wild-type XP55 (a) and SLSs in non-chemotactic mutant KI-5 (b) cells. (c), The collision of 2 independent SLSs. (d), Dose dependency of KI-5 cell density on SLS formation. All pictures were taken at the indicated time after exhaustion of the D. discoideum food source, Klebsiella aerogenes.

Figure 2. Failure of SLS formation in non-chemotactic mutants with defective cAMP signalling, and the effect of cAMP and DIF-1 on SLS formation.

(a), Absence of multicellular structure formation in carA, gbpB, and acaA null mutants following bacterial exhaustion. (b), SLS formation with 1 mM cAMP. (c), Absence of SLS formation with 4 mM caffeine. (d), SLS formation with 100 μM DIF-1.

Figure 3. Cell movements in SLSs.

(a), Cell movement of SLSs. (b), Cell movement of SLSs with RFP-labelled KI-5 cells. (c), Removal of cells in front of a moving SLS. The arrow and arrowhead indicate cells incorporated into and left behind an SLS, respectively.

Figure 4. Collision of two independent SLSs with RFP-expressing KI-5 cells.

The arrow and arrowhead indicate cells which maintained and changed direction, respectively, in SLSs after collision.

Figure 5. Movement of the dispersed cells derived from SLSs.

(a), Cell movement of loosely disaggregated SLS. Arrows indicate breakage of a cell concatenate. Arrowheads indicate attachment of 2 cell concatenates. (b), SLS formation on an agar plate containing 5 mM EDTA.