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. 2021 Aug 25;7(35):eabh2278.
doi: 10.1126/sciadv.abh2278. Print 2021 Aug.

The environment topography alters the way to multicellularity in Myxococcus xanthus

Corina H Ramos  1   2 , Edna Rodríguez-Sánchez  2 , Juan Antonio Arias Del Angel  2 , Alejandro V Arzola  3 , Mariana Benítez  2 , Ana E Escalante  2 , Alessio Franci  1 , Giovanni Volpe  4 , Natsuko Rivera-Yoshida  5   2
Affiliations

The environment topography alters the way to multicellularity in Myxococcus xanthus

Corina H Ramos et al. Sci Adv. .

Abstract

The social soil-dwelling bacterium Myxococcus xanthus can form multicellular structures, known as fruiting bodies. Experiments in homogeneous environments have shown that this process is affected by the physicochemical properties of the substrate, but they have largely neglected the role of complex topographies. We experimentally demonstrate that the topography alters single-cell motility and multicellular organization in M. xanthus In topographies realized by randomly placing silica particles over agar plates, we observe that the cells' interaction with particles drastically modifies the dynamics of cellular aggregation, leading to changes in the number, size, and shape of the fruiting bodies and even to arresting their formation in certain conditions. We further explore this type of cell-particle interaction in a computational model. These results provide fundamental insights into how the environment topography influences the emergence of complex multicellular structures from single cells, which is a fundamental problem of biological, ecological, and medical relevance.

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Figures

Fig. 1
Fig. 1. M. xanthus fruiting-body development in homogeneous and heterogeneous topographies.
M. xanthus cells come together to develop multicellular fruiting bodies, which can be identified as dark spots on agar plates. (A) On a homogeneous substrate and at a cellular density of 0.01 OD, fruiting bodies start forming at 72 hours and are completely mature by 96 hours (some mature fruiting bodies are indicated by the arrows). (B and C) Even a relatively small amount of silica particles randomly distributed over the agar surface can (B) hinder (0.7% particle packing fraction) or (C) completely prevent (7.5% particle packing fraction) the fruiting-body formation. Scale bar, 1 mm.
Fig. 2
Fig. 2. Fruiting-body formation depends on cell and particle density.
(A) Micrographs at 96 hours of M. xanthus populations generated over agar substrates at different particle densities (0, 0.7, 4.2, 7.5, 24, 36, and 45% packing fractions) and at different cellular densities (0.01, 0.02, 0.06, 0.1, 0.3, 0.7 OD at 550 nm). For each condition, the micrograph shows the central section of the population. The large dark spots are the mature fruiting bodies (FBs), while the small dots in the background are the silica particles dispersed over the agar substrate. Scale bar, 1 mm. (B to E) Mean variation of fruiting-body developmental traits as a function of cellular and particle density: (B) number, (C) average size of the five biggest fruiting bodies, (D) average size of the five smallest fruiting bodies, and (E) circularity as a shape descriptor. In all cases, the region within the pink line indicates the set of conditions in which fruiting-body formation is completely arrested. See also movie S1.
Fig. 3
Fig. 3. M. xanthus cell-cell and cell-particle local interactions during cellular aggregation.
(A) Initial configuration of some cells (elongated bright shapes) and particles (dark discs with bright spot). The gray rings around the silica particles are the aqueous menisci. (B) Movement of cells near the particle during 2 hours [corresponding to the top frame in (A)]. The white dotted lines indicate the contact line of the aqueous meniscus (larger circle, rp) and the surface of the particle (smaller circle, r0). The colored lines correspond to the trajectories of cells moving toward the particle; colors go from cold to warm according to the time when each position was recorded. Note that the cells’ trajectories tend to overlap, which reflects that the cells follow the slime trails left by other cells. (C) Movement of cells far away from particles during 2 hours [corresponding to the bottom frame in (A)]. The white dotted lines indicate the contact line of the aqueous meniscus of the bacterial aggregate (larger outline, rb) and the surface of the aggregate (smaller outline, r0). The colored lines correspond to the trajectories of cells moving toward cellular aggregates (note that some target aggregates moved from their initial position during the 2 hours); the color code is the same as in (B). (D and E) Average speed of tracked cells while they approach (D) a particle and (E) other cells [corresponding to the trajectories in (B) and (C), respectively]. The gray-shaded areas represent 1 SD. r0 and rp correspond to the surface and meniscus of the target particle or bacterial aggregate in (D) and (E), respectively. Scale bars, 10 μm. See movie S2.
Fig. 4
Fig. 4. Effect of particle attraction in simulations of cellular aggregation.
(A) Simulation of M. xanthus cellular aggregation on a smooth and homogeneous substrate at 5000 Monte Carlo steps. (B and C) Corresponding simulation on a heterogeneous substrate varying the packing fraction (1, 5, 15, and 25%) of (B) non-attractive and (C) attractive particles. Particles are shown in gray. Cells not trapped by particles are shown in yellow, and cells trapped by particles are shown in light gray. Scale bar, 10 μm. (D) Quantification of the number of aggregated cells, normalized to the aggregation numbers on the homogeneous substrate. The number of cells that are not trapped by particles drastically diminishes as the density of attractive particles increases, while it remains almost unchanged as the density of non-attractive particles increases. See movie S3.
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