The idiosyncrasy of spatial structure in bacterial competition

BMC Research Notes

Juan E Keymer²  Cees Dekker¹  Rutger G Woolthuis¹  Peter Galajda³  Felix J H Hol¹ 

[1] Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Lorentzweg 1, Delft, 2628 CJ, The Netherlands;Institute of Physics, Faculty of Physics, P. Catholic University of Chile, Ave. Vicuña Mackenna 4860, Macul, Santiago, Chile;Institute of Biophysics, Biological Research Centre of the Hungarian Academy of Sciences, Temesvari krt. 62, Szeged, Hungary

关键词: Cooperation;    Bacterial competition;    Spatial structure;   

Others  :  1231962
DOI  :  10.1186/s13104-015-1169-x

 received in 2014-04-22, accepted in 2015-05-13,  发布年份 2015

【 摘 要 】

Background

The spatial structure of a habitat can have a strong impact on community dynamics. Different experimental approaches exist to explore the effect of spatial structure on bacterial communities. To investigate the effect of ‘space’, a single implementation of spatial structure is often contrasted to bacterial community dynamics in well-mixed cultures. While such comparisons are useful, it is likely that the observed dynamics will be particular to the specific experimental implementation of spatial structure. In order to address this question, we track the community dynamics of a two-strain Escherichia coli community in various spatial habitats and relate the observed dynamics to the structure of a habitat.

Results

By tracking the community dynamics of rpoS wild-type and mutant E. coli in radially expanding colonies on solid and semi-solid agar plates, we find that the mutant strain outcompetes the wild-type on semi-solid agar plates, whereas the two strains coexist on solid agar. We compare these results to previous studies in which the same two strains were shown to coexist in habitats spatially structured by microfabrication, while the mutant outcompeted the wild-type in well-mixed batch cultures. Together, these observations show that different implementations of space may result in qualitatively different community dynamics. Furthermore, we argue that the same competitive outcome (e.g. coexistence) may arise from distinct underlying dynamics in different experimental implementations of spatial structure.

Conclusions

Our observations demonstrate that different experimental implementations of spatial structure may not only lead to quantitatively different communities (changes in the relative abundance of types) but can also lead to qualitatively different outcomes of long-term community dynamics (coexistence versus extinction and loss of biodiversity).

【 授权许可】

   
2015 Hol et al.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Dieckmann U, Law R, Metz JA: The geometry of ecological interactions: simplifying spatial complexity. Cambridge University Press, Cambridge; 2000.
• [2]Durrett R, Levin S: The importance of being discrete (and spatial). Theor Popul Biol 1994, 46(3):363-394.
• [3]Griffin A, West S, Buckling A: Cooperation and competition in pathogenic bacteria. Nature 2004, 430(7003):1024-1027.
• [4]Nahum JR, Harding BN, Kerr B: Evolution of restraint in a structured rock-paper-scissors community. Proc Natl Acad Sci USA 2011, 108(Suppl 2):10831-8.
• [5]Datta MS, Korolev KS, Cvijovic I, Dudley C, Gore J: Range expansion promotes cooperation in an experimental microbial metapopulation. Proc Natl Acad Sci 2013, 110(18):7354-7359.
• [6]Hallatschek O, Hersen P, Ramanathan S, Nelson DR: Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci 2007, 104(50):19926-19930.
• [7]Van Dyken JD, Müller MJ, Mack KM, Desai MM: Spatial population expansion promotes the evolution of cooperation in an experimental prisoner’s dilemma. Curr Biol 2013, 23:919-923.
• [8]Müller MJ, Neugeboren BI, Nelson DR, Murray AW: Genetic drift opposes mutualism during spatial population expansion. Proc Natl Acad Sci 2014, 111:1037-1042.
• [9]Korolev KS, Xavier JB, Nelson DR, Foster KR: A quantitative test of population genetics using spatiogenetic patterns in bacterial colonies. Am Nat 2011, 178(4):538.
• [10]Rudge TJ, Federici F, Steiner PJ, Kan A, Haseloff J: Cell polarity-driven instability generates self-organized, fractal patterning of cell layers. ACS Synth Biol 2013, 2:705-714.
• [11]Keymer J, Galajda P, Muldoon C, Park S, Austin R: Bacterial metapopulations in nanofabricated landscapes. Proc Natl Acad Sci USA 2006, 103(46):17290-17295.
• [12]Hol FJ, Galajda P, Nagy K, Woolthuis RG, Dekker C, Keymer JE: Spatial structure facilitates cooperation in a social dilemma: Empirical evidence from a bacterial community. PloS One 2013, 8(10):77042.
• [13]Connell JL, Ritschdorff ET, Whiteley M, Shear JB: 3D printing of microscopic bacterial communities. Proc Natl Acad Sci USA 2013, 110(46):18380-5.
• [14]Drescher K, Nadell CD, Stone HA, Wingreen NS, Bassler BL: Solutions to the public goods dilemma in bacterial biofilms. Curr Biol 2014, 24(1):50-5.
• [15]van Vliet S, Hol FJH, Weenink T, Galajda P, Keymer JE: The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations. BMC Microbiol 2014, 14:116. BioMed Central Full Text
• [16]Hol FJ, Voges MJ, Dekker C, Keymer JE: Nutrient-responsive regulation determines biodiversity in a colicin-mediated bacterial community. BMC Biol 2014, 12(1):68. BioMed Central Full Text
• [17]Weber MF, Poxleitner G, Hebisch E, Frey E, Opitz M: Chemical warfare and survival strategies in bacterial range expansions. J R Soc Interface 2014, 11(96):20140172.
• [18]Hol FJH, Dekker C: Zooming in to see the bigger picture: microfluidic and nanofabrication tools to study bacteria. Science 2014, 346(6208):1251821.
• [19]Nowak M, May R: Evolutionary games and spatial chaos. Nature 1992, 359(6398):826-829.
• [20]Lion S, Baalen M: Self-structuring in spatial evolutionary ecology. Ecol Lett 2008, 11(3):277-295.
• [21]Kreft J-U: Biofilms promote altruism. Microbiology 2004, 150(8):2751-2760.
• [22]Santos F, Pacheco J, Lenaerts T: Evolutionary dynamics of social dilemmas in structured heterogeneous populations. Proc Natl Acad Sci USA 2006, 103(9):3490-3494.
• [23]Doebeli M, Hauert C: Models of cooperation based on the prisoner’s dilemma and the snowdrift game. Ecol Lett 2005, 8(7):748-766.
• [24]Nadell C, Foster K, Xavier J: Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 2010, 6(3):1000716.
• [25]Hauert C, Doebeli M: Spatial structure often inhibits the evolution of cooperation in the snowdrift game. Nature 2004, 428(6983):643-646.
• [26]Verbruggen E, El Mouden C, Jansa J, Akkermans G, Bücking H, West SA, et al.: Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism. Am Nat 2012, 179(5):133-146.
• [27]Allen B, Gore J, Nowak MA (2013) Spatial dilemmas of diffusible public goods. eLife 2
• [28]Zambrano M, Siegele D, Almiron M, Tormo A, Kolter R: Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 1993, 259(5102):1757-1760.
• [29]Vulic M, Kolter R: Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics 2001, 158(2):519-26.
• [30]Finkel SE, Kolter R: Evolution of microbial diversity during prolonged starvation. Proc Natl Acad Sci 1999, 96(7):4023-4027.
• [31]Finkel S: Long-term survival during stationary phase: evolution and the gasp phenotype. Nat Rev Microbiol 2006, 4(2):113-120.
• [32]Keymer JE, Galajda P, Lambert G, Liao D, Austin RH: Computation of mutual fitness by competing bacteria. Proc Natl Acad Sci USA 2008, 105(51):20269-73.
• [33]Lambert G, Liao D, Vyawahare S, Austin RH: Anomalous spatial redistribution of competing bacteria under starvation conditions. J Bacteriol 2011, 193(8):1878-83.
• [34]Kussell E: Evolution in microbes. Ann Rev Biophys 2013, 42:493-514.
• [35]Patten C, Kirchhof M, Schertzberg M, Morton R, Schellhorn H: Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 2004, 272(5):580-591.
• [36]Dong T, Kirchhof M, Schellhorn H: Rpos regulation of gene expression during exponential growth of Escherichia coli k12. Mol Genet Genomics 2008, 279(3):267-277.
• [37]Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N (2010) Computer control of microscopes using μManager. Curr Protoc Mol Biol 14.20.1–14.20.17