A link between cell movement and gene expression argues that motility is required for cell-cell signaling during fruiting body development.

Abstract

Nonmotile mutants of Myxococcus xanthus (Myxobacterales) failed to execute the morphogenetic movements required to shape a fruiting body. In addition, nonmotile mutants produced very few spores when plated for fruiting body development at cell densities appropriate for wild-type cells. At higher initial cell densities, the proportion of nonmotile cells that sporulate increased, indicating that one important function of motility in fruiting body development is to increase the local cell density. However, even at 10 times normal cell density, nonmotile cells sporulated at only 1% the wild-type level. This sporulation deficiency of nonmotile mutants accompanies an altered pattern of gene expression, monitored by using transcriptional fusions of lacZ to genes expressed at specific times during fruiting body development. Motility was not required for normal expression of five lac fusions that are expressed within the first 6 hr of fruiting-body development. However, the levels of expression from five lac fusions to later-expressed genes were reduced or abolished in nonmotile strains. [3-Galactosidase expression in these late Tn5 lac insertions was increased, and fruiting body development occurred in certain nonmotile strains that can be stimulated to move when mixed with a donor strain. This shows that motility itself is required because the stimulated cells are nonmotile genotypically. The nonmotile mutations had the same effect on developmental [3-galactosidase expression from these 10 lac fusions as an insertion mutation in the csg (formerly spoC) gene. csg mutants have a cell-cell interaction defect that blocks fruiting body development at -6 hr. The similarity in the pattern of developmental expression of motility mutants and csg mutants suggests that motility is required for this csg-mediated cell-cell interaction.

C-factor has distinct aggregation and sporulation thresholds during Myxococcus development

“…1 and 2). Within aggregates, the local C-factor concentration would be expected to increase with cell density and with the increased efficiency of cell-to-cell C-factor transmission (9,10).…”

Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus

“…The direction of movement of a chain is determined by the cell at the leading end of the chain and is conveyed from cell to cell by the end-to-end contacts. At the high cell density, cells tend to stay in side-by-side contact with each other (21,23,24). Cell movement in chains may create alignment of neighboring cells, thus giving rise to the formation of secondary chains, which are associated with the initiating chains by the lateral side-by-side contacts.…”

“…The C-signal induces aggregation and sporulation in a concentration-dependent manner, i.e., intermediate level aggregation is induced and at high levels sporulation is induced (13)(14)(15). C-signal transmission occurs by a contactdependent mechanism (12) that involves end-to-end contacts between cells and fails when cells are unable to make these even though they are able to make side-by-side contacts (21)(22)(23)(24).…”

C factor, a cell-surface-associated intercellular signaling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus.

“…However, the aggregation, sporulation, and developmental gene expression of a csgA mutant is rescued by codevelopment with wild-type (wt) cells or by addition of purified C factor at 1 nM (5,6). Rescue by wt cells requires the motility of both cell types (17,18). It has been suggested that movement establishes specific contacts between cells (thought to be end-to-end contacts) that are required for intercellular C-factor signal transmission (19,20).…”