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Link to original content: http://www.ncbi.nlm.nih.gov/pubmed/27303375
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Review
. 2016 May 26:7:781.
doi: 10.3389/fmicb.2016.00781. eCollection 2016.

Myxobacteria: Moving, Killing, Feeding, and Surviving Together

Affiliations
Review

Myxobacteria: Moving, Killing, Feeding, and Surviving Together

José Muñoz-Dorado et al. Front Microbiol. .

Abstract

Myxococcus xanthus, like other myxobacteria, is a social bacterium that moves and feeds cooperatively in predatory groups. On surfaces, rod-shaped vegetative cells move in search of the prey in a coordinated manner, forming dynamic multicellular groups referred to as swarms. Within the swarms, cells interact with one another and use two separate locomotion systems. Adventurous motility, which drives the movement of individual cells, is associated with the secretion of slime that forms trails at the leading edge of the swarms. It has been proposed that cellular traffic along these trails contributes to M. xanthus social behavior via stigmergic regulation. However, most of the cells travel in groups by using social motility, which is cell contact-dependent and requires a large number of individuals. Exopolysaccharides and the retraction of type IV pili at alternate poles of the cells are the engines associated with social motility. When the swarms encounter prey, the population of M. xanthus lyses and takes up nutrients from nearby cells. This cooperative and highly density-dependent feeding behavior has the advantage that the pool of hydrolytic enzymes and other secondary metabolites secreted by the entire group is shared by the community to optimize the use of the degradation products. This multicellular behavior is especially observed in the absence of nutrients. In this condition, M. xanthus swarms have the ability to organize the gliding movements of 1000s of rods, synchronizing rippling waves of oscillating cells, to form macroscopic fruiting bodies, with three subpopulations of cells showing division of labor. A small fraction of cells either develop into resistant myxospores or remain as peripheral rods, while the majority of cells die, probably to provide nutrients to allow aggregation and spore differentiation. Sporulation within multicellular fruiting bodies has the benefit of enabling survival in hostile environments, and increases germination and growth rates when cells encounter favorable conditions. Herein, we review how these social bacteria cooperate and review the main cell-cell signaling systems used for communication to maintain multicellularity.

Keywords: Myxococcus xanthus; motility; multicellularity; predation; prokaryotic development.

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Figures

FIGURE 1
FIGURE 1
Myxococcus xanthus multicellular cell cycle. (A) Vegetative growth. In the presence of nutrients cells move in a coordinated manner, forming swarms. When swarms make contact with the prey, cells penetrates the prey colony and lyse the cells. (B) Developmental cycle. Upon starvation, cells moving collectively initiate a developmental program and exchange extracellular signals as well as physical contact signals to first form aggregates and later build millimeter-long upright fruiting bodies filled with differentiated, reproductive and environmentally resistant cells called myxospores (rounds cells), surrounded by two other subpopulations showing division of labor: a monolayer of aligned non-reproductive peripheral rods (yellow rod cells) and cells that undergo altruistic obligatory autolysis by programmed cell death (light brown rod cells). Myxospores ensure survival during starvation or desiccation and can be dispersed to other environments and germinate when nutrient conditions ameliorate.
FIGURE 2
FIGURE 2
M. xanthus A and S motility. (A) The edge of a M. xanthus swarm. Upper circle, single cells (with A-motility); bottom circle, group of cells (with S-motility). (B) Phase contrast microscopy revealing A-motility-mediated trails observed at the leading edge. Migration of other cells through these trails promotes the formation of dense regions of aligned cells and favors intimate cell–cell contacts. (C) Proposed focal adhesion (FA) model of gliding motility. The cytoplasmic, inner membrane and periplasmic components of the Agl–Glt motility protein complex move along a helical track (provided by cytoskeletal proteins) within the cells. After this trafficking, the complex engages the outer components and then the entire complex adheres to the substrate via ECM slime, forming an FA that allows the machinery to push. The protein complexes translocate along the cellular track, pushing the cell forward. (D,E) Components of the S-motility system, fibrils and type IV pili (T4P). (D) Scanning electron microscopy of the meshwork of fibrils that maintain cellular cohesion. (E) Atomic force microscopy of T4P localized at the leading cell pole. (F) Proposed model for S-motility. T4P anchors to the EPS present on neighboring cells and propels the cell by cycles of extension, attachment, and retraction. The pictures of the phase bright A-motility trails (B) and T4P (E) were adapted from Gloag et al. (2015) with permission of the authors, and from Pelling et al. (2005) with permission; copyright (2005) National Academy of Sciences, USA. Micrograph of the fibril material was kindly provided by L. J. Shimkets.
FIGURE 3
FIGURE 3
Myxococcus xanthus multicellular behaviors. (A) M. xanthus DK1622 coordinated movements (rippling) induced by Sinorhizobium meliloti AK70 (SmAK70) during predation. (B) OMV chains cryofixed and visualized by transmission electronic microscopy. OMVs contain multiple hydrolytic enzymes and secondary metabolites indicating an important role in killing and lysis of prey. (C) Scanning electron micrographs of the interface DK1622 (Mx) versus Streptomyces coelicolor M45 (Sc) cells after 96 h of incubation. The magnified picture shows the intense ECM connection between the attacking cells. (D) Frontal attack strategy: M. xanthus DK1622 (Mx) versus a non-mucoid colony of S. meliloti 8530W (Sm8530W). (E) Wolf pack attack strategy: M. xanthus DZ2 (Mx) versus a mucoid colony of S. meliloti AK21 (SmAK21). (F) M. xanthus DZF1 fruiting body formation after 72 h on starvation medium. (G–I) Scanning microscopy of M. xanthus DZF1 fruiting body showing the round spores and the surrounding peripheral rods. (H,I) Within the fruiting bodies, the myxospores are firmly bound together by a cohesive ECM. Picture (B) has been adapted from Remis et al. (2014) with permission, copyright 2013 Society for Applied Microbiology and John Wiley & Sons Ltd.

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