Abstract
The feeding efficiency of microbial predators depends on both the availability of various prey species and abiotic variables. Myxococcus xanthus is a bacterial predator that searches for microbial prey by gliding motility, and then kills and lyses its prey with secreted compounds. We manipulated three ecological variables to examine their effects on the predatory performance of M. xanthus to better understand its behavior and how it affects prey populations. Experiments were designed to determine how surface solidity (hard vs soft agar), density of prey patches (1 vs 2 cm grids), and type of prey (Gram-positive Micrococcus luteus vs Gram-negative Escherichia coli) affect predatory swarming and prey killing by M. xanthus. The prey were dispersed in patches on a buffered agar surface. M. xanthus swarms attacked a greater proportion of prey patches when patches were densely arranged on a hard-agar surface, compared with either soft-agar surfaces or low-patch-density arrangements. These ecological variables did not significantly influence the rate of killing of individual prey within a patch, although a few surviving prey were more likely to be recovered on soft agar than on hard agar. These results indicate that M. xanthus quickly kills most nearby E. coli or M. luteus regardless of the surface. However, the ability of M. xanthus to search out patches of these prey is affected by surface hardness, the density of prey patches, and the prey species.
Similar content being viewed by others
References
Alexander, M (1981) Why microbial predators and parasites do not eliminate their prey and hosts. Annu Rev Microbiol 35: 113–133
Bohannan, BJM, Lenski, RE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3: 362–377
Bretscher, AP, Kaiser, D (1978) Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J Bacteriol 133: 763–768
Bull, CT, Shetty, KG, Subbarao, KV (2002) Interactions between Myxobacteria, plant pathogenic fungi, and biocontrol agents. Plant Dis 86: 889–896
Carlton, BC, Brown, BJ (1981) Gene mutation. In: Gerhardt, P, Murray, R, Costilow, R, Nester, E, Wood, W, Krigg, N, Philips, G (Eds.) Manual of Methods for General Bacteriology. American Society for Microbiology, Washington, D.C., pp 222–242
Dworkin, M (1996) Recent advances in the social and developmental biology of the Myxobacteria. Microbiol Rev 60: 70–102
Estes, JA, Tinker, MT, Williams, TM, Doak, DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282: 473–476
Fiegna, F, Velicer, GJ (2005) Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol 3: 1980–1987
Fontes, M, Kaiser, D (1999) Myxococcus cells respond to elastic forces in their substrate. Proc Natl Acad Sci U S A 96: 8052–8057
Hart, BA, Zahler, SA (1966) Lytic enzyme produced by Myxococcus xanthus. J Bacteriol 92: 1632–1637
Hillesland, KL, Velicer, GJ (2005) Resource level affects relative performance of the two motility systems of Myxococcus xanthus. Microb Ecol 49: 558–566
Hodgkin, J, Kaiser, D (1979) Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet 171: 177–191
Holling, CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91: 385–398
Jackson, L, Whiting, RC (1992) Reduction of an Escherichia coli K12 population by Bdellovibrio bacteriovorus under various in vitro conditions of parasite:host ratio, temperature, or pH. J Food Protect 55: 859–861
Jurgens, K, Matz, C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie van Leeuwenhoek 81: 413–434
Kaiser, D (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A 76: 5952–5956
Kaiser, D (2003) Coupling cell movement to multicellular development in Myxobacteria. Nat Rev Microbiol 1: 45–54
Kearns, DB, Shimkets, LJ (2001) Lipid chemotaxis and signal transduction in Myxococcus xanthus. Trends Microbiol 9: 126–129
Martin, MO (2002) Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4: 467–477
Messier, F (1994) Ungulate population models with predation: a case study with the North American moose. Ecology 75: 478–488
Mittelbach, GG, Turner, AM, Hall, DJ, Rettig, JE, Osenberg, CW (1995) Perturbation and resilience: a long-term, whole lake study of predator extinction and reintroduction. Ecology 76: 2347–2360
Pham, VD, Shebelut, CW, Diodati, ME, Bull, CT, Singer, M (2005) Mutations affecting predation ability of the soil bacterium Myxococcus xanthus. Microbiology 151: 1865–1874
Reichenbach, H, Gerth, K, Irschik, H, Kunze, B, Höfle, G (1988) Myxobacteria: a source of new antibiotics. TIBTECH 6: 115–121
Reichenbach, H, Höfle, G (1993) Biologically active secondary metabolites from Myxobacteria. Biotechnol Adv 11: 219–277
Rønn, R, McCaig, AE, Griffiths, BS, Prosser, JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68: 6094–6105
Rosenberg, E, Vaks, B, Zuckerberg, A (1973) Bactericidal action of an antibiotic produced by Myxococcus xanthus. Antimicrob Agents Chemother 4: 507–513
Rosenberg, E, Varon, M (1984) Antibiotics and lytic enzymes. In: Rosenberg, E (Ed.) Myxobacteria: Development and Cell Interactions. Springer-Verlag, New York, pp 109–125
Sambrook, J, Fritsch, E, Maniatis, T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Plainview, NY
SAS Institute (2001) The SAS System. SAS Institute, Cary, NC
Schmitz, OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151: 327–342
Shi, W, Zusman, DR (1993) The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc Natl Acad Sci U S A 90: 3378–3382
Spiller, DA, Schoener, TW (1998) Lizards reduce spider species richness by excluding rare species. Ecology 79: 503–516
Spormann, AM (1999) Gliding motility in bacteria: insights from studies of Myxococcus xanthus. Microbiol Mol Biol Rev 63: 621–641
Stenseth, NC, Shabbar, A, Chan, KS, Boutin, S, Rueness, EK, Ehrich, D, Hurrell, JW, Lingjærde, OC, Jakobsen, KS (2004) Snow conditions may create an invisible barrier for lynx. Proc Natl Acad Sci U S A 101: 10632–10634
Sudo, S, Dworkin, M (1972) Bacteriolytic enzymes produced by Myxococcus xanthus. J Bacteriol 110: 236–245
Sun, H, Zusman, DR, Shi, W (2000) Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol 10: 1143–1146
Varon, M, Zeigler, BP (1978) Bacterial predator–prey interaction at low prey density. Appl Environ Microbiol 36: 11–17
Varon, M, Fine, M, Stein, A (1984) The maintenance of Bdellovibrio at low prey density. Microb Ecol 10: 95–98
Velicer, GJ, Kroos, L, Lenski, RE (1998) Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc Natl Acad Sci U S A 95: 12376–12380
Vlamakis, HC, Kirby, JR, Zusman, DR (2004) The Che4 pathway of Myxococcus xanthus regulates type IV pilus-mediated motility. Mol Microbiol 52: 1799–1811
Wolgemuth, C, Hoiczyk, E, Kaiser, D, Oster, G (2002) How Myxobacteria glide. Curr Biol 12: 369–377
Yang, Z, Geng, Y, Xu, D, Kaplan, HB, Shi, W (1998) A new set of chemotaxis homologues is essential for Myxococcus xanthus social motility. Mol Microbiol 30: 1123–1130
Yang, Z, Ma, X, Tong, L, Kaplan, HB, Shimkets, LJ, Shi, W (2000) Myxococcus xanthus dif genes are required for biogenesis of cell surface fibrils essential for social gliding motility. J Bacteriol 182: 5793–5798
Acknowledgments
We thank Neerja Hajela for technical assistance, and members of the Lenski and Velicer groups for valuable discussion. This research was supported by a grant from the U.S. National Science Foundation (R.E. Lenski).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hillesland, K.L., Lenski, R.E. & Velicer, G.J. Ecological Variables Affecting Predatory Success in Myxococcus xanthus . Microb Ecol 53, 571–578 (2007). https://doi.org/10.1007/s00248-006-9111-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-006-9111-3