Higher temperatures generically favour slower-growing bacterial species in multispecies communities.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
01
07
2019
accepted:
27
01
2020
pubmed:
4
3
2020
medline:
25
6
2020
entrez:
4
3
2020
Statut:
ppublish
Résumé
Temperature is one of the fundamental environmental variables that determine the composition and function of microbial communities. However, a predictive understanding of how microbial communities respond to changes in temperature is lacking, partly because it is not obvious which aspects of microbial physiology determine whether a species could benefit from a change in the temperature. Here we incorporate how microbial growth rates change with temperature into a modified Lotka-Volterra competition model and predict that higher temperatures should-in general-favour the slower-growing species in a bacterial community. We experimentally confirm this prediction in pairwise cocultures assembled from a diverse set of species and show that these changes to pairwise outcomes with temperature are also predictive of changing outcomes in three-species communities, suggesting that our theory may be applicable to more-complex assemblages. Our results demonstrate that it is possible to predict how bacterial communities will shift with temperature knowing only the growth rates of the community members. These results provide a testable hypothesis for future studies of more-complex natural communities and we hope that this work will help to bridge the gap between ecological theory and the complex dynamics observed in metagenomic surveys.
Identifiants
pubmed: 32123319
doi: 10.1038/s41559-020-1126-5
pii: 10.1038/s41559-020-1126-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
560-567Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM102311
Pays : United States
Références
Gilbert, J. A. et al. Defining seasonal marine microbial community dynamics. ISME J. 6, 298–308 (2012).
Fuhrman, J. A., Cram, J. A. & Needham, D. M. Marine microbial community dynamics and their ecological interpretation. Nat. Rev. Microbiol. 13, 133–146 (2015).
Ward, C. S. et al. Annual community patterns are driven by seasonal switching between closely related marine bacteria. ISME J. 11, 1412–1422 (2017).
Fuhrman, J. A. et al. A latitudinal diversity gradient in planktonic marine bacteria. Proc. Natl Acad. Sci. USA 105, 7774–7778 (2008).
Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).
Deslippe, J. R., Hartmann, M., Simard, S. W. & Mohn, W. W. Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol. Ecol. 82, 303–315 (2012).
Luo, C. et al. Soil microbial community responses to a decade of warming as revealed by comparative metagenomics. Appl. Environ. Microbiol. 80, 1777–1786 (2014).
Jiang, L. & Morin, P. J. Temperature fluctuation facilitates coexistence of competing species in experimental microbial communities. J. Anim. Ecol. 76, 660–668 (2007).
Descamps-Julien, B. & Gonzalez, A. Stable coexistence in a fluctuating environment: an experimental demonstration. Ecology 86, 2815–2824 (2005).
Abreu, C. I., Friedman, J., Andersen Woltz, V. L. & Gore, J. Mortality causes universal changes in microbial community composition. Nat. Commun. 10, 2120 (2019).
Ratkowsky, D. A., Olley, J., McMeekin, T. A. & Ball, A. Relationship between temperature and growth rate of bacterial cultures. J. Bacteriol. 149, 1–5 (1982).
Rosso, L., Lobry, J. R. & Flandrois, J. P. An unexpected correlation between cardinal temperatures of microbial growth highlighted by a new model. J. Theor. Biol. 162, 447–463 (1993).
Friedman, J., Higgins, L. M. & Gore, J. Community structure follows simple assembly rules in microbial microcosms. Nat. Ecol. Evol. 1, 0109 (2017).
Stubbendieck, R. M. & Straight, P. D. Multifaceted interfaces of bacterial competition. J. Bacteriol. 198, 2145–2155 (2016).
Ratzke, C. & Gore, J. Modifying and reacting to the environmental pH can drive bacterial interactions. PLoS Biol. 16, e2004248 (2018).
De Carvalho, C. C. R. & Fernandes, P. Production of metabolites as bacterial responses to the marine environment. Mar. Drugs 8, 705–727 (2010).
James, P. D. A., Edwards, C. & Dawson, M. The effects of temperature, pH and growth rate on secondary metabolism in Streptomyces thermoviolaceus grown in a chemostat. J. Gen. Microbiol. 137, 1715–1720 (1991).
Sun, W., Qian, X., Gu, J., Wang, X.-J. & Duan, M.-L. Mechanism and effect of temperature on variations in antibiotic resistance genes during anaerobic digestion of dairy manure. Sci. Rep. 6, 30237 (2016).
Kim, C., Wilkins, K., Bowers, M., Wynn, C. & Ndegwa, E. Influence of pH and temperature on growth characteristics of leading foodborne pathogens in a laboratory medium and select food beverages. Austin Food Sci. 3, 1031 (2018).
Lewington-Pearce, L. et al. Temperature-dependence of minimum resource requirements alters competitive hierarchies in phytoplankton. Oikos 128, 1194–1205 (2019).
doi: 10.1111/oik.06060
Hanke, A. et al. Selective pressure of temperature on competition and cross-feeding within denitrifying and fermentative microbial communities. Front. Microbiol. 6, 1461 (2016).
Lax, S., Abreu, C. I. & Gore, J. Higher temperatures generically favor slower-growing bacterial species in multispecies communities. Figshare https://doi.org/10.6084/m9.figshare.8285543.v1 (2020).