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1. Growth rate as a link between microbial diversity and soil biogeochemistry

   https://doi.org/10.1038/s41559-024-02520-7  

   Foley, Megan M; Stone, Bram_W G; Caro, Tristan A; Sokol, Noah W; Koch, Benjamin J; Blazewicz, Steven J; Dijkstra, Paul; Hayer, Michaela; Hofmockel, Kirsten; Finley, Brianna K; et al (November 2024, Nature Ecology & Evolution)

   Measuring the growth rate of a microorganism is a simple yet profound way to quantify its effect on the world. The absolute growth rate of a microbial population reflects rates of resource assimilation, biomass production and element transformation—some of the many ways in which organisms affect Earth’s ecosystems and climate. Microbial fitness in the environment depends on the ability to reproduce quickly when conditions are favourable and adopt a survival physiology when conditions worsen, which cells coordinate by adjusting their relative growth rate. At the population level, relative growth rate is a sensitive metric of fitness, linking survival and reproduction to the ecology and evolution of populations. Techniques combining omics and stable isotope probing enable sensitive measurements of the growth rates of microbial assemblages and individual taxa in soil. Microbial ecologists can explore how the growth rates of taxa with known traits and evolutionary histories respond to changes in resource availability, environmental conditions and interactions with other organisms. We anticipate that quantitative and scalable data on the growth rates of soil microorganisms, coupled with measurements of biogeochemical fluxes, will allow scientists to test and refine ecological theory and advance process-based models of carbon flux, nutrient uptake and ecosystem productivity. Measurements of in situ microbial growth rates provide insights into the ecology of populations and can be used to quantitatively link microbial diversity to soil biogeochemistry. 

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2. Life history strategies among soil bacteria—dichotomy for few, continuum for many

   https://doi.org/10.1038/s41396-022-01354-0  

   Stone, Bram_W_G; Dijkstra, Paul; Finley, Brianna_K; Fitzpatrick, Raina; Foley, Megan_M; Hayer, Michaela; Hofmockel, Kirsten_S; Koch, Benjamin_J; Li, Junhui; Liu, Xiao_Jun_A; et al (February 2023, The ISME Journal)

   Abstract Study of life history strategies may help predict the performance of microorganisms in nature by organizing the complexity of microbial communities into groups of organisms with similar strategies. Here, we tested the extent that one common application of life history theory, the copiotroph-oligotroph framework, could predict the relative population growth rate of bacterial taxa in soils from four different ecosystems. We measured the change of in situ relative growth rate to added glucose and ammonium using both 18O–H2O and 13C quantitative stable isotope probing to test whether bacterial taxa sorted into copiotrophic and oligotrophic groups. We saw considerable overlap in nutrient responses across most bacteria regardless of phyla, with many taxa growing slowly and few taxa that grew quickly. To define plausible life history boundaries based on in situ relative growth rates, we applied Gaussian mixture models to organisms’ joint 18O–13C signatures and found that across experimental replicates, few taxa could consistently be assigned as copiotrophs, despite their potential for fast growth. When life history classifications were assigned based on average relative growth rate at varying taxonomic levels, finer resolutions (e.g., genus level) were significantly more effective in capturing changes in nutrient response than broad taxonomic resolution (e.g., phylum level). Our results demonstrate the difficulty in generalizing bacterial life history strategies to broad lineages, and even to single organisms across a range of soils and experimental conditions. We conclude that there is a continued need for the direct measurement of microbial communities in soil to advance ecologically realistic frameworks. 

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3. The interplay of phenotypic variability and fitness in finite microbial populations

   https://doi.org/10.1098/rsif.2019.0827  

   Levien, Ethan; Kondev, Jane; Amir, Ariel (May 2020, Journal of The Royal Society Interface)

   In isogenic microbial populations, phenotypic variability is generated by a combination of stochastic mechanisms, such as gene expression, and deterministic factors, such as asymmetric segregation of cell volume. Here we address the question: how does phenotypic variability of a microbial population affect its fitness? While this question has previously been studied for exponentially growing populations, the situation when the population size is kept fixed has received much less attention, despite its relevance to many natural scenarios. We show that the outcome of competition between multiple microbial species can be determined from the distribution of phenotypes in the culture using a generalization of the well-known Euler–Lotka equation, which relates the steady-state distribution of phenotypes to the population growth rate. We derive a generalization of the Euler–Lotka equation for finite cultures, which relates the distribution of phenotypes among cells in the culture to the exponential growth rate. Our analysis reveals that in order to predict fitness from phenotypes, it is important to understand how distributions of phenotypes obtained from different subsets of the genealogical history of a population are related. To this end, we derive a mapping between the various ways of sampling phenotypes in a finite population and show how to obtain the equivalent distributions from an exponentially growing culture. Finally, we use this mapping to show that species with higher growth rates in exponential growth conditions will have a competitive advantage in the finite culture. 

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4. Decreased growth of wild soil microbes after 15 years of transplant‐induced warming in a montane meadow

   https://doi.org/10.1111/gcb.15911  

   Purcell, Alicia M.; Hayer, Michaela; Koch, Benjamin J.; Mau, Rebecca L.; Blazewicz, Steven J.; Dijkstra, Paul; Mack, Michelle C.; Marks, Jane C.; Morrissey, Ember M.; Pett‐Ridge, Jennifer; et al (October 2021, Global Change Biology)

   Abstract The carbon stored in soil exceeds that of plant biomass and atmospheric carbon and its stability can impact global climate. Growth of decomposer microorganisms mediates both the accrual and loss of soil carbon. Growth is sensitive to temperature and given the vast biological diversity of soil microorganisms, the response of decomposer growth rates to warming may be strongly idiosyncratic, varying among taxa, making ecosystem predictions difficult. Here, we show that 15 years of warming by transplanting plant–soil mesocosms down in elevation, strongly reduced the growth rates of soil microorganisms, measured in the field using undisturbed soil. The magnitude of the response to warming varied among microbial taxa. However, the direction of the response—reduced growth—was universal and warming explained twofold more variation than did the sum of taxonomic identity and its interaction with warming. For this ecosystem, most of the growth responses to warming could be explained without taxon‐specific information, suggesting that in some cases microbial responses measured in aggregate may be adequate for climate modeling. Long‐term experimental warming also reduced soil carbon content, likely a consequence of a warming‐induced increase in decomposition, as warming‐induced changes in plant productivity were negligible. The loss of soil carbon and decreased microbial biomass with warming may explain the reduced growth of the microbial community, more than the direct effects of temperature on growth. These findings show that direct and indirect effects of long‐term warming can reduce growth rates of soil microbes, which may have important feedbacks to global warming. 

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5. Rapid growth rate responses of terrestrial bacteria to field warming on the Antarctic Peninsula

   https://doi.org/10.1038/s41396-023-01536-4  

   Purcell, Alicia M.; Dijkstra, Paul; Hungate, Bruce A.; McMillen, Kelly; Schwartz, Egbert; van Gestel, Natasja (October 2023, The ISME Journal)

   Abstract Ice-free terrestrial environments of the western Antarctic Peninsula are expanding and subject to colonization by new microorganisms and plants, which control biogeochemical cycling. Measuring growth rates of microbial populations and ecosystem carbon flux is critical for understanding how terrestrial ecosystems in Antarctica will respond to future warming. We implemented a field warming experiment in early (bare soil; +2 °C) and late (peat moss-dominated; +1.2 °C) successional glacier forefield sites on the western Antarctica Peninsula. We used quantitative stable isotope probing with H218O using intact cores in situ to determine growth rate responses of bacterial taxa to short-term (1 month) warming. Warming increased the growth rates of bacterial communities at both sites, even doubling the number of taxa exhibiting significant growth at the early site. Growth responses varied among taxa. Despite that warming induced a similar response for bacterial relative growth rates overall, the warming effect on ecosystem carbon fluxes was stronger at the early successional site—likely driven by increased activity of autotrophs which switched the ecosystem from a carbon source to a carbon sink. At the late-successional site, warming caused a significant increase in growth rate of many Alphaproteobacteria, but a weaker and opposite gross ecosystem productivity response that decreased the carbon sink—indicating that the carbon flux rates were driven more strongly by the plant communities. Such changes to bacterial growth and ecosystem carbon cycling suggest that the terrestrial Antarctic Peninsula can respond fast to increases in temperature, which can have repercussions for long-term elemental cycling and carbon storage. 

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