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Title: Short-range C-signaling restricts cheating behavior during Myxococcus xanthus development
ABSTRACT Myxococcus xanthususes short-range C-signaling to coordinate multicellular mound formation with sporulation during fruiting body development. AcsgAmutant deficient in C-signaling can cheat on wild type (WT) in mixtures and form spores disproportionately, but our understanding of cheating behavior is incomplete. We subjected mixtures of WT andcsgAcells at different ratios to co-development and used confocal microscopy and image analysis to quantify the arrangement and morphology of cells. At a ratio of one WT to fourcsgAcells (1:4), mounds failed to form. At 1:2, only a few mounds and spores formed. At 1:1, mounds formed with a similar number and arrangement of WT andcsgArods early in development, but later the number ofcsgAspores near the bottom of these nascent fruiting bodies (NFBs) exceeded that of WT. This cheating after mound formation involvedcsgAforming spores at a greater rate, while WT disappeared at a greater rate, either lysing or exiting NFBs. At 2:1 and 4:1,csgArods were more abundant than expected throughout the biofilm both before and during mound formation, and cheating continued after mound formation. We conclude that C-signaling restricts cheating behavior by requiring sufficient WT cells in mixtures. Excess cheaters may interfere with positive feedback loops that depend on the cellular arrangement to enhance C-signaling during mound building. Since long-range signaling could not likewise communicate the cellular arrangement, we propose that C-signaling was favored evolutionarily and that other short-range signaling mechanisms provided selective advantages in bacterial biofilm and multicellular animal development. IMPORTANCEBacteria communicate using both long- and short-range signals. Signaling affects community composition, structure, and function. Adherent communities called biofilms impact medicine, agriculture, industry, and the environment. To facilitate the manipulation of biofilms for societal benefits, a better understanding of short-range signaling is necessary. We investigated the susceptibility of short-range C-signaling to cheating duringMyxococcus xanthusbiofilm development. A mutant deficient in C-signaling fails to form mounds containing spores (i.e., fruiting bodies) but cheats on C-signaling by wild type in starved cell mixtures and forms spores disproportionately. We found that cheating requires sufficient wild-type cells in the initial mix and can occur both before mound formation and later during the sporulation stage of development. By restricting cheating behavior, short-range C-signaling may have been favored evolutionarily rather than long-range diffusible signaling. Cheating restrictions imposed by short-range signaling may have likewise driven the evolution of multicellularity broadly.  more » « less
Award ID(s):
1951025
PAR ID:
10596790
Author(s) / Creator(s):
; ; ;
Editor(s):
Søgaard-Andersen, Lotte
Publisher / Repository:
American Society for Microbiology
Date Published:
Journal Name:
mBio
Volume:
15
Issue:
11
ISSN:
2150-7511
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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