Latent functional diversity may accelerate microbial community responses to temperature fluctuations
Curation statements for this article:-
Curated by eLife
eLife Assessment:
This manuscript will be of interest to microbial ecologists and biogeochemists working on soil carbon cycling and responses to climate warming. This study uses an elegant experiment to show that standing variation, both phylogenetic and phenotypic, enables microbial community adaptation to higher temperatures. The authors' conclusions are supported by the data, and this work lays a foundation for future experimental and modeling studies.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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- Ecology (eLife)
Abstract
How complex microbial communities respond to climatic fluctuations remains an open question. Due to their relatively short generation times and high functional diversity, microbial populations harbor great potential to respond as a community through a combination of strain-level phenotypic plasticity, adaptation, and species sorting. However, the relative importance of these mechanisms remains unclear. We conducted a laboratory experiment to investigate the degree to which bacterial communities can respond to changes in environmental temperature through a combination of phenotypic plasticity and species sorting alone. We grew replicate soil communities from a single location at six temperatures between 4°C and 50°C. We found that phylogenetically and functionally distinct communities emerge at each of these temperatures, with K -strategist taxa favored under cooler conditions and r -strategist taxa under warmer conditions. We show that this dynamic emergence of distinct communities across a wide range of temperatures (in essence, community-level adaptation) is driven by the resuscitation of latent functional diversity: the parent community harbors multiple strains pre-adapted to different temperatures that are able to ‘switch on’ at their preferred temperature without immigration or adaptation. Our findings suggest that microbial community function in nature is likely to respond rapidly to climatic temperature fluctuations through shifts in species composition by resuscitation of latent functional diversity.
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eLife Assessment:
This manuscript will be of interest to microbial ecologists and biogeochemists working on soil carbon cycling and responses to climate warming. This study uses an elegant experiment to show that standing variation, both phylogenetic and phenotypic, enables microbial community adaptation to higher temperatures. The authors' conclusions are supported by the data, and this work lays a foundation for future experimental and modeling studies.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
In this manuscript, Smith et al. evaluate whether phenotypic plasticity and/or species sorting (changes in community composition) occur during a four-week-long incubation of a single soil at a range of temperatures. By using a relatively simple setup and restricting their cultivation to relatively fast-growing taxa well-suited to growth in the lab, the authors were able to measure a commendable number of traits and successfully evaluate the thermal niche of the majority of organisms tested. The authors did a very thorough job of explaining how they came to the conclusion that species sorting is the dominant driver of community-level adaptation to temperature in their experiment, and they do an outstanding job using other literature to support and contextualize these conclusions. I also commend the authors …
Reviewer #1 (Public Review):
In this manuscript, Smith et al. evaluate whether phenotypic plasticity and/or species sorting (changes in community composition) occur during a four-week-long incubation of a single soil at a range of temperatures. By using a relatively simple setup and restricting their cultivation to relatively fast-growing taxa well-suited to growth in the lab, the authors were able to measure a commendable number of traits and successfully evaluate the thermal niche of the majority of organisms tested. The authors did a very thorough job of explaining how they came to the conclusion that species sorting is the dominant driver of community-level adaptation to temperature in their experiment, and they do an outstanding job using other literature to support and contextualize these conclusions. I also commend the authors for not overstating the relevance of their results and sticking to the conclusion that this is a possible range of responses rather than concluding that the patterns observed for these taxa are representative of how dominant soil bacteria are responding. Overall this is a very good paper and sets the stage well for future work in, for instance, constraining community turnover vs. acclimation in trait-based carbon cycling models.
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Reviewer #2 (Public Review):
Overall the experimental design is clearly explained and well justified. While there has been much speculation about the mechanisms to explain variation in how communities of microbes respond to environmental change, this study uses an experimental approach to show convincingly that selection on standing variation in ecological strategies among members of a microbial community is likely to explain the ability of these communities to rapidly shift in composition and function in response to variation in temperature. A particular strength of the manuscript is that the authors measured phenotypes, functions, and phylogenetic relationships among the strains being studied. This allowed them to illustrate that there is phylogenetic signal in the phenotypes, functions, and temperature responses of microbial strains, …
Reviewer #2 (Public Review):
Overall the experimental design is clearly explained and well justified. While there has been much speculation about the mechanisms to explain variation in how communities of microbes respond to environmental change, this study uses an experimental approach to show convincingly that selection on standing variation in ecological strategies among members of a microbial community is likely to explain the ability of these communities to rapidly shift in composition and function in response to variation in temperature. A particular strength of the manuscript is that the authors measured phenotypes, functions, and phylogenetic relationships among the strains being studied. This allowed them to illustrate that there is phylogenetic signal in the phenotypes, functions, and temperature responses of microbial strains, in order to fully understand the responses of the communities to temperature treatments. The authors' claims and conclusions - that community responses to temperature were driven by shifts in the abundance of strains to resuscitate latent functional diversity within communities - were supported by their data.
Weaknesses of the study include the fact that the culture-based approach to quantifying communities may have missed important aspects of community-level diversity that could be missed by this culture-based approach. Some microbial taxa, especially in soils, are extremely difficult to grow in culture. Thus, the community of strains observed for some communities could be missing important taxa present in the communities in the wild. This potential bias is not likely to change the authors' conclusions, but it would be worth thinking about and discussing the potential impact of this bias on the interpretation of the study.
Overall this study makes an important contribution to the field by revealing the patterns of phenotypic evolution within microbial communities, and by showing that species sorting (rather than immigration, adaptation, or phenotypic plasticity) is the mechanism that is likely to explain the ability of microbial communities to rapidly adapt to changing environments.
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