Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast - PubMed (original) (raw)
Comparative Study
Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast
Dominika M Wloch-Salamon et al. Proc Biol Sci. 2008.
Abstract
The ecological role of interference competition through toxin production is not well understood. In particular, it is unclear under what conditions the benefits of toxic killing outweigh the metabolic costs involved. A killer advantage has been suggested to rely on local competitive interactions where the benefits of killing accrue to the toxin producer preferentially, but this notion has little empirical support. In addition, contrasting predictions exist about the effect of resource abundance on the benefits of toxin production; this benefit should either be highest when resources are abundant and metabolic costs are relatively low or when resources are scarce and toxic killing is a 'last resort strategy' to obtain nutrients. Here, we test these predictions for one aspect of competitive ability, that is, the ability of toxin producers to invade a population of sensitive non-producers from a low initial frequency. We use competition experiments between isogenic K1 toxin-producing and non-producing strains of Saccharomyces cerevisiae, where we manipulate dispersal under two extreme nutrient conditions: one environment with and the other without replenishment of nutrients. We find that toxin production is beneficial when dispersal is limited under both nutrient conditions, but only when resources are abundant these outweigh its cost and allow invasion of the producer.
Figures
Figure 1
Fitness of the killer (K), sensitive (S) and control (C) strains relative to a resistant reference strain measured in direct competition in the Nut+ Dis+ environment with at least 20-fold replication. C and K carry the same genetic marker (grey bars), which is different from that of S (white bar). Error bars represent 95% CIs.
Figure 2
Trajectories of the log ratio of K versus S and C versus S densities during the 80 days of competition in three replicate populations in four environments: (a) Nut+ _Dis_−, (b) Nut+ Dis+, (c) _Nut_− _Dis_− and (d) _Nut_− Dis+ environment. Closed symbols are for K/S and open symbols for C/S. The dashed line in (b) shows the expected trajectory based on the resource competitive difference between K and S only (i.e. without the effect of toxic killing). To estimate the frequency of K and S in the _Nut_− environment, populations had to be destroyed, and hence the trajectories reflect the average and s.e. of three different replicate populations for each time point.
Figure 3
Assay of toxic killing in the _Nut_− environment. The change in frequency of both the strains (S, white bars and K, grey bars) in competition relative to monoculture in four constitutive intervals during the 21 days of the experiment is shown. (a) Dis+ environment and (b) _Dis_− environment. Error bars reflect the s.e. based on pseudovalues from the jackknife procedure (see §2).
Similar articles
- Density-dependent effects on allelopathic interactions in yeast.
Greig D, Travisano M. Greig D, et al. Evolution. 2008 Mar;62(3):521-7. doi: 10.1111/j.1558-5646.2007.00292.x. Epub 2007 Nov 3. Evolution. 2008. PMID: 17983463 - The costs and benefits of killer toxin production by the yeast Pichia kluyveri.
Pintar J, Starmer WT. Pintar J, et al. Antonie Van Leeuwenhoek. 2003;83(1):89-97. doi: 10.1023/a:0000000089097. Antonie Van Leeuwenhoek. 2003. PMID: 12755485 - Competition and allelopathy with resource storage: two resources.
Grover JP, Wang FB. Grover JP, et al. J Theor Biol. 2014 Jun 21;351:9-24. doi: 10.1016/j.jtbi.2014.02.013. Epub 2014 Feb 21. J Theor Biol. 2014. PMID: 24560723 - Susceptibility of individual cells of Saccharomyces cerevisiae to the killer toxin K1.
Bartunek M, Jelinek O, Vondrejs V. Bartunek M, et al. Biochem Biophys Res Commun. 2001 May 4;283(2):526-30. doi: 10.1006/bbrc.2001.4809. Biochem Biophys Res Commun. 2001. PMID: 11327733 - The Ecology and Evolution of Microbial Competition.
Ghoul M, Mitri S. Ghoul M, et al. Trends Microbiol. 2016 Oct;24(10):833-845. doi: 10.1016/j.tim.2016.06.011. Epub 2016 Aug 18. Trends Microbiol. 2016. PMID: 27546832 Review.
Cited by
- Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa.
Inglis RF, Brown SP, Buckling A. Inglis RF, et al. Evolution. 2012 Nov;66(11):3472-84. doi: 10.1111/j.1558-5646.2012.01706.x. Epub 2012 Jul 3. Evolution. 2012. PMID: 23106711 Free PMC article. - Spite and virulence in the bacterium Pseudomonas aeruginosa.
Inglis RF, Gardner A, Cornelis P, Buckling A. Inglis RF, et al. Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5703-7. doi: 10.1073/pnas.0810850106. Epub 2009 Mar 24. Proc Natl Acad Sci U S A. 2009. PMID: 19321425 Free PMC article. - Application of high resolution melting assay (HRM) to study temperature-dependent intraspecific competition in a pathogenic bacterium.
Ashrafi R, Bruneaux M, Sundberg LR, Pulkkinen K, Ketola T. Ashrafi R, et al. Sci Rep. 2017 Apr 20;7(1):980. doi: 10.1038/s41598-017-01074-y. Sci Rep. 2017. PMID: 28428555 Free PMC article. - Resource use of soilborne Streptomyces varies with location, phylogeny, and nitrogen amendment.
Schlatter DC, DavelosBaines AL, Xiao K, Kinkel LL. Schlatter DC, et al. Microb Ecol. 2013 Nov;66(4):961-71. doi: 10.1007/s00248-013-0280-6. Microb Ecol. 2013. PMID: 23959115 - Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes.
Kinkel LL, Schlatter DC, Xiao K, Baines AD. Kinkel LL, et al. ISME J. 2014 Feb;8(2):249-56. doi: 10.1038/ismej.2013.175. Epub 2013 Oct 24. ISME J. 2014. PMID: 24152720 Free PMC article.
References
- Baganz F, Hayes A, Marren D, Gardner D.C.J, Oliver S.G. Suitability of replacement markers for functional analysis studies in Saccharomyces cerevisiae. Yeast. 1997;13:1563–1573. doi:10.1002/(SICI)1097-0061(199712)13:16<1563::AID-YEA240>3.0.CO;2-6 - DOI - PubMed
- Brown S.P, Le Chat L, De Paepe M, Taddei F. Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 2006;16:2048–2052. doi:10.1016/j.cub.2006.08.089 - DOI - PubMed
- Carreiro S.C, Pagnocca F.C, Bacci M, Jr, Bueno O.C, Hebling M.J, Middelhoven W.J. Occurrence of killer yeasts in leaf-cutting ant nests. Folia Microbiol. (Praha) 2002;47:259–262. - PubMed
- Case T.J, Gilpin M.E. Interference competition and niche theory. Proc. Natl Acad. Sci. USA. 1974;71:3073–3077. doi:10.1073/pnas.71.8.3073 - DOI - PMC - PubMed
- Chao L, Levin B.R. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl Acad. Sci. USA. 1981;78:6324–6328. doi:10.1073/pnas.78.10.6324 - DOI - PMC - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Molecular Biology Databases