Multicellular Development in Myxococcus xanthus Is Stimulated by Predator-Prey Interactions

ABSTRACT Myxococcus xanthus is a predatory bacterium that exhibits complex social behavior. The most pronounced behavior is the aggregation of cells into raised fruiting body structures in which cells differentiate into stress-resistant spores. In the laboratory, monocultures of M. xanthus at a very high density will reproducibly induce hundreds of randomly localized fruiting bodies when exposed to low nutrient availability and a solid surface. In this report, we analyze how M. xanthus fruiting body development proceeds in a coculture with suitable prey. Our analysis indicates that when prey bacteria are provided as a nutrient source, fruiting body aggregation is more organized, such that fruiting bodies form specifically after a step-down or loss of prey availability, whereas a step-up in prey availability inhibits fruiting body formation. This localization of aggregates occurs independently of the basal nutrient levels tested, indicating that starvation is not required for this process. Analysis of early developmental signaling relA and asgD mutants indicates that they are capable of forming fruiting body aggregates in the presence of prey, demonstrating that the stringent response and A-signal production are surprisingly not required for the initiation of fruiting behavior. However, these strains are still defective in differentiating to spores. We conclude that fruiting body formation does not occur exclusively in response to starvation and propose an alternative model in which multicellular development is driven by the interactions between M. xanthus cells and their cognate prey.

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β-d-Allose Inhibits Fruiting Body Formation and Sporulation in Myxococcus xanthus

Journal of Bacteriology ◽

10.1128/jb.00792-06 ◽

2006 ◽

Vol 189 (1) ◽

pp. 169-178 ◽

Cited By ~ 7

Author(s):

Marielena Chavira ◽

Nga Cao ◽

Karen Le ◽

Tanveer Riar ◽

Navid Moradshahi ◽

...

Keyword(s):

Fruiting Body ◽

Myxococcus Xanthus ◽

Fruiting Body Formation ◽

Submerged Cultures ◽

Multicellular Development ◽

Body Formation ◽

Body Development ◽

Phenotype Microarrays ◽

Glucose Phosphorylation ◽

High Concentrations

ABSTRACT Myxococcus xanthus, a gram-negative soil bacterium, responds to amino acid starvation by entering a process of multicellular development which culminates in the assembly of spore-filled fruiting bodies. Previous studies utilizing developmental inhibitors (such as methionine, lysine, or threonine) have revealed important clues about the mechanisms involved in fruiting body formation. We used Biolog phenotype microarrays to screen 384 chemicals for complete inhibition of fruiting body development in M. xanthus. Here, we report the identification of a novel inhibitor of fruiting body formation and sporulation, β-d-allose. β-d-Allose, a rare sugar, is a member of the aldohexose family and a C3 epimer of glucose. Our studies show that β-d-allose does not affect cell growth, viability, agglutination, or motility. However, β-galactosidase reporters demonstrate that genes activated between 4 and 14 h of development show significantly lower expression levels in the presence of β-d-allose. Furthermore, inhibition of fruiting body formation occurs only when β-d-allose is added to submerged cultures before 12 h of development. In competition studies, high concentrations of galactose and xylose antagonize the nonfruiting response to β-d-allose, while glucose is capable of partial antagonism. Finally, a magellan-4 transposon mutagenesis screen identified glcK, a putative glucokinase gene, required for β-d-allose-mediated inhibition of fruiting body formation. Subsequent glucokinase activity assays of the glcK mutant further supported the role of this protein in glucose phosphorylation.

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Aggregation during Fruiting Body Formation in Myxococcus xanthus Is Driven by Reducing Cell Movement

Journal of Bacteriology ◽

10.1128/jb.01206-06 ◽

2006 ◽

Vol 189 (2) ◽

pp. 611-619 ◽

Cited By ~ 27

Author(s):

Oleksii Sliusarenko ◽

David R. Zusman ◽

George Oster

Keyword(s):

Fruiting Body ◽

Myxococcus Xanthus ◽

Cell Movement ◽

Fruiting Bodies ◽

Fruiting Body Formation ◽

Agent Based ◽

Body Formation ◽

Early Stages ◽

Cell Velocity ◽

Reversal Frequency

ABSTRACT When starved, Myxococcus xanthus cells assemble themselves into aggregates of about 105 cells that grow into complex structures called fruiting bodies, where they later sporulate. Here we present new observations on the velocities of the cells, their orientations, and reversal rates during the early stages of fruiting body formation. Most strikingly, we find that during aggregation, cell velocities slow dramatically and cells orient themselves in parallel inside the aggregates, while later cell orientations are circumferential to the periphery. The slowing of cell velocity, rather than changes in reversal frequency, can account for the accumulation of cells into aggregates. These observations are mimicked by a continuous agent-based computational model that reproduces the early stages of fruiting body formation. We also show, both experimentally and computationally, how changes in reversal frequency controlled by the Frz system mutants affect the shape of these early fruiting bodies.

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New Locus Important for Myxococcus Social Motility and Development

Journal of Bacteriology ◽

10.1128/jb.00942-07 ◽

2007 ◽

Vol 189 (21) ◽

pp. 7937-7941 ◽

Cited By ~ 7

Author(s):

Cui-ying Zhang ◽

Ke Cai ◽

Hong Liu ◽

Yong Zhang ◽

Hong-wei Pan ◽

...

Keyword(s):

Fruiting Body ◽

Myxococcus Xanthus ◽

Gliding Motility ◽

Salt Tolerant ◽

Fruiting Body Formation ◽

Body Formation ◽

Homologous Genes ◽

Body Development ◽

Fruiting Body Development ◽

Social Motility

ABSTRACT The mts locus in salt-tolerant Myxococcus fulvus HW-1 was found to be critical for gliding motility, fruiting-body formation, and sporulation. The homologous genes in Myxococcus xanthus are also important for social motility and fruiting-body development. The mts genes were determined to be involved in cell-cell cohesion in both myxobacterial species.

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Transcript Profiling Reveals Novel Marker Genes Involved in Fruiting Body Formation in Tuber borchii

Eukaryotic Cell ◽

10.1128/ec.4.9.1599-1602.2005 ◽

2005 ◽

Vol 4 (9) ◽

pp. 1599-1602 ◽

Cited By ~ 25

Author(s):

Silvia Gabella ◽

Simona Abbà ◽

Sebastien Duplessis ◽

Barbara Montanini ◽

Francis Martin ◽

...

Keyword(s):

Fruiting Body ◽

Marker Genes ◽

Fruiting Bodies ◽

Fruiting Body Formation ◽

Tuber Borchii ◽

Body Formation ◽

Physiological Processes ◽

Body Development ◽

Fruiting Body Development ◽

Two Stages

ABSTRACT cDNA arrays were used to explore mechanisms controlling fruiting body development in the truffle Tuber borchii. Differences in gene expression were higher between reproductive and vegetative stage than between two stages of fruiting body maturation. We suggest hypotheses about the importance of various physiological processes during the development of fruiting bodies.

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Developmental Aggregation of Myxococcus xanthus Requires frgA, anfrz-Related Gene

Journal of Bacteriology ◽

10.1128/jb.182.23.6614-6621.2000 ◽

2000 ◽

Vol 182 (23) ◽

pp. 6614-6621 ◽

Cited By ~ 12

Author(s):

Kyungyun Cho ◽

Anke Treuner-Lange ◽

Kathleen A. O'Connor ◽

David R. Zusman

Keyword(s):

Fruiting Body ◽

Myxococcus Xanthus ◽

Complex Life Cycle ◽

Fruiting Bodies ◽

Related Gene ◽

Wild Type ◽

Fruiting Body Formation ◽

Body Formation ◽

Extracellular Signals ◽

Directed Motility

ABSTRACT Myxococcus xanthus is a gram-negative bacterium which has a complex life cycle that includes multicellular fruiting body formation. Frizzy mutants are characterized by the formation of tangled filaments instead of hemispherical fruiting bodies on fruiting agar. Mutations in the frz genes have been shown to cause defects in directed motility, which is essential for both vegetative swarming and fruiting body formation. In this paper, we report the discovery of a new gene, called frgA (forfrz-related gene), which confers a subset of the frizzy phenotype when mutated. The frgA null mutant showed reduced swarming and the formation of frizzy aggregates on fruiting agar. However, this mutant still displayed directed motility in a spatial chemotaxis assay, whereas the majority offrz mutants fail to show directed movements in this assay. Furthermore, the frizzy phenotype of the frgA mutant could be complemented extracellularly by wild-type cells or strains carrying non-frz mutations. The phenotype of the frgAmutant is similar to that of the abcA mutant and suggests that both of these mutants could be defective in the production or export of extracellular signals required for fruiting body formation rather than in the sensing of such extracellular signals. ThefrgA gene encodes a large protein of 883 amino acids which lacks homologues in the databases. The frgA gene is part of an operon which includes two additional genes, frgBand frgC. The frgB gene encodes a putative histidine protein kinase, and the frgC gene encodes a putative response regulator. The frgB and frgCnull mutants, however, formed wild-type fruiting bodies.

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The Myxococcus xanthus Nla4 Protein Is Important for Expression of Stringent Response-Associated Genes, ppGpp Accumulation, and Fruiting Body Development

Journal of Bacteriology ◽

10.1128/jb.00894-07 ◽

2007 ◽

Vol 189 (23) ◽

pp. 8474-8483 ◽

Cited By ~ 12

Author(s):

Faisury Ossa ◽

Michelle E. Diodati ◽

Nora B. Caberoy ◽

Krista M. Giglio ◽

Mick Edmonds ◽

...

Keyword(s):

Fruiting Body ◽

Expression Patterns ◽

Myxococcus Xanthus ◽

Stringent Response ◽

Fruiting Body Formation ◽

Body Development ◽

Normal Expression ◽

Fruiting Body Development ◽

Coordinated Expression ◽

Low Levels

ABSTRACT Changes in gene expression are important for the landmark morphological events that occur during Myxococcus xanthus fruiting body development. Enhancer binding proteins (EBPs), which are transcriptional activators, play prominent roles in the coordinated expression of developmental genes. A mutation in the EBP gene nla4 affects the timing of fruiting body formation, the morphology of mature fruiting bodies, and the efficiency of sporulation. In this study, we showed that the nla4 mutant accumulates relatively low levels of the stringent nucleotide ppGpp. We also found that the nla4 mutant is defective for early developmental events and for vegetative growth, phenotypes that are consistent with a deficiency in ppGpp accumulation. Further studies revealed that nla4 cells produce relatively low levels of GTP, a precursor of RelA-dependent synthesis of (p)ppGpp. In addition, the normal expression patterns of all stringent response-associated genes tested, including the M. xanthus ppGpp synthetase gene relA, are altered in nla4 mutant cells. These findings indicate that Nla4 is part of regulatory pathway that is important for mounting a stringent response and for initiating fruiting body development.

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Spatial Organization of Myxococcus xanthus during Fruiting Body Formation

Journal of Bacteriology ◽

10.1128/jb.01008-07 ◽

2007 ◽

Vol 189 (24) ◽

pp. 9126-9130 ◽

Cited By ~ 38

Author(s):

Patrick D. Curtis ◽

Rion G. Taylor ◽

Roy D. Welch ◽

Lawrence J. Shimkets

Keyword(s):

Fruiting Body ◽

Spatial Organization ◽

Myxococcus Xanthus ◽

Matrix Material ◽

Cell Monolayer ◽

Fruiting Bodies ◽

Fruiting Body Formation ◽

Quiescent Phase ◽

Body Development ◽

Uppermost Layer

ABSTRACT Microcinematography was used to examine fruiting body development of Myxococcus xanthus. Wild-type cells progress through three distinct phases: a quiescent phase with some motility but little aggregation (0 to 8 h), a period of vigorous motility leading to raised fruiting bodies (8 to 16 h), and a period of maturation during which sporulation is initiated (16 to 48 h). Fruiting bodies are extended vertically in a series of tiers, each involving the addition of a cell monolayer on top of the uppermost layer. A pilA (MXAN_5783) mutant produced less extracellular matrix material and thus allowed closer examination of tiered aggregate formation. A csgA (MXAN_1294) mutant exhibited no quiescent phase, aberrant aggregation in phase 2, and disintegration of the fruiting bodies in the third phase.

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FibA and PilA act cooperatively during fruiting body formation of Myxococcus xanthus

Molecular Microbiology ◽

10.1111/j.1365-2958.2006.05298.x ◽

2006 ◽

Vol 61 (5) ◽

pp. 1283-1293 ◽

Cited By ~ 17

Author(s):

Pamela J. Bonner ◽

Wesley P. Black ◽

Zhaomin Yang ◽

Lawrence J. Shimkets

Keyword(s):

Fruiting Body ◽

Myxococcus Xanthus ◽

Fruiting Body Formation ◽

Body Formation

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Social selection within aggregative multicellular development drives morphological evolution

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2021.1522 ◽

2021 ◽

Vol 288 (1963) ◽

Author(s):

Marco La Fortezza ◽

Gregory J. Velicer

Keyword(s):

Fruiting Body ◽

Morphological Evolution ◽

Social Process ◽

Treatment Level ◽

Fruiting Bodies ◽

Fruiting Body Formation ◽

Multicellular Development ◽

Cellular Environment ◽

Unicellular Organisms ◽

Complex Forms

Aggregative multicellular development is a social process involving complex forms of cooperation among unicellular organisms. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies and often unfolds within genetically and behaviourally diverse conspecific cellular environments. Here, we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes its morphological evolution. We manipulated the cellular composition of Myxococcus development in an experiment in which evolving populations initiated from a single ancestor repeatedly co-developed with one of several non-evolving partners—a cooperator, three cheaters and three antagonists. Fruiting body morphology was found to diversify not only as a function of partner genotype but more broadly as a function of partner social character, with antagonistic partners selecting for greater fruiting body formation than cheaters or the cooperator. Yet even small degrees of genetic divergence between distinct cheater partners sufficed to drive treatment-level morphological divergence. Co-developmental partners also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In summary, we find that even just a few genetic differences affecting developmental and social features can greatly impact morphological evolution of multicellular bodies and experimentally demonstrate that microbial warfare can promote cooperation.

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