DOI: 10.1128/jb.00544-07. Multicellular Development in <i>Myxococcus xanthus</i> Is Stimulated by Predator-Prey Interactions

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

10.1128/jb.00544-07

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

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.

Bibliography

Berleman, J. E., & Kirby, J. R. (2007). Multicellular Development in Myxococcus xanthus Is Stimulated by Predator-Prey Interactions. Journal of Bacteriology, 189(15), 5675â5682.

Authors 2

James E. Berleman (first)
John R. Kirby (additional)

References 29 Referenced 54

10.1128/JB.00559-06
Braeken, K., M. Moris, R. Daniels, J. Vanderleyden, and J. Michiels. 2006. New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol. 14 : 45-54. (10.1016/j.tim.2005.11.006) / Trends Microbiol. (2006)
Cho, K., and D. R. Zusman. 1999. Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol. Microbiol. 34 : 714-725. (10.1046/j.1365-2958.1999.01633.x) / Mol. Microbiol. (1999)
10.1128/jb.86.1.67-72.1963
Fontes, M., and D. Kaiser. 1999. Myxococcus cells respond to elastic forces in their substrate. Proc. Natl. Acad. Sci. USA 96 : 8052-8057. (10.1073/pnas.96.14.8052) / Proc. Natl. Acad. Sci. USA (1999)
Hagen, D. C., A. P. Bretscher, and D. Kaiser. 1978. Synergism between morphogenetic mutants of Myxococcus xanthus. Dev. Biol 64 : 284-296. (10.1016/0012-1606(78)90079-9) / Dev. Biol (1978)
Harris, B. Z., D. Kaiser, and M. Singer. 1998. The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes Dev. 12 : 1022-1035. (10.1101/gad.12.7.1022) / Genes Dev. (1998)
Kaiser, D. 2004. Signaling in myxobacteria. Annu. Rev. Microbiol. 58 : 75-98. (10.1146/annurev.micro.58.030603.123620) / Annu. Rev. Microbiol. (2004)
10.1128/jb.171.5.2762-2772.1989
10.1128/jb.174.10.3319-3326.1992
10.1128/jb.174.22.7360-7369.1992
10.1128/jb.176.17.5341-5349.1994
McBride, M. J., R. A. Weinberg, and D. R. Zusman. 1989. “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc. Natl. Acad. Sci. USA 86 : 424-428. (10.1073/pnas.86.2.424) / Proc. Natl. Acad. Sci. USA (1989)
Mignot, T., J. W. Shaevitz, P. L. Hartzell, and D. R. Zusman. 2007. Evidence that focal adhesion complexes power bacterial gliding motility. Science 315 : 853-856. (10.1126/science.1137223) / Science (2007)
10.1128/jb.173.11.3318-3333.1991
Oetker, H. 1953. Studies on the nutrition of various myxobacteria. Arch. Mikrobiol. 19 : 206-246. (10.1007/BF00446400) / Arch. Mikrobiol. (1953)
10.1128/jb.174.10.3311-3318.1992
Rasmussen, A. A., S. L. Porter, J. P. Armitage, and L. Sogaard-Andersen. 2005. Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Mol. Microbiol. 56 : 1358-1372. (10.1111/j.1365-2958.2005.04629.x) / Mol. Microbiol. (2005)
Reichenbach, H. 1966. Myxococcus spp. (Myxobacteriales) Schwarmentwicklung und bildung von protocysten, p. 557-578. In G. Wolf (ed.), Encyclop. Cinematogr. Film E778/1965. / Encyclop (1966)
Rosenberg, E., and M. Varon. 1984. Antibiotics and lytic enzymes, p. 109-125. In E. Rosenberg (ed.), Myxobacteria: development and cell interactions. Springer, New York, NY. / Myxobacteria: development and cell interactions (1984)
Molecular cloning: a laboratory manual 1989
Shimkets, L. J. 1999. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu. Rev. Microbiol. 53 : 525-549. (10.1146/annurev.micro.53.1.525) / Annu. Rev. Microbiol. (1999)
10.1128/jb.152.1.451-461.1982
Singer, M., and D. Kaiser. 1995. Ectopic production of guanosine penta- and tetraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Genes Dev. 9 : 1633-1644. (10.1101/gad.9.13.1633) / Genes Dev. (1995)
10.1128/JB.01206-06
Sun, H., D. R. Zusman, and W. Shi. 2000. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10 : 1143-1146. (10.1016/S0960-9822(00)00705-3) / Curr. Biol. (2000)
Thaxter, R. 1892. On the Myxobacteriaceae, a new order of Schizomycetes. Bot. Gaz. 17 : 389-406. (10.1086/326866) / Bot. Gaz. (1892)
10.1128/JB.181.1.24-33.1999
10.1146/annurev.cellbio.21.012704.131001

Dates

Type	When
Created	18 years, 3 months ago (May 19, 2007, 10:27 a.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:35 p.m.)
Indexed	1 month ago (Aug. 5, 2025, 8:21 a.m.)
Issued	18 years, 1 month ago (Aug. 1, 2007)
Published	18 years, 1 month ago (Aug. 1, 2007)
Published Print	18 years, 1 month ago (Aug. 1, 2007)

Funders 0

None

BibTeX

@article{Berleman_2007, title={Multicellular Development in Myxococcus xanthus Is Stimulated by Predator-Prey Interactions}, volume={189}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.00544-07}, DOI={10.1128/jb.00544-07}, number={15}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Berleman, James E. and Kirby, John R.}, year={2007}, month=aug, pages={5675–5682} }

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