All organisms are sensitive to the abiotic environment, and a deteriorating environment can cause extinction. However, survival in a multispecies community depends upon interactions, and some species may even be favored by a harsh environment that impairs others, leading to potentially surprising community transitions as environments deteriorate. Here we combine theory and laboratory microcosms to predict how simple microbial communities will change under added mortality, controlled by varying dilution. We find that in a two-species coculture, increasing mortality favors the faster grower, confirming a theoretical prediction. Furthermore, if the slower grower dominates under low mortality, the outcome can reverse as mortality increases. We find that this tradeoff between growth and competitive ability is prevalent at low dilution, causing outcomes to shift dramatically as dilution increases, and that these two-species shifts propagate to simple multispecies communities. Our results argue that a bottom-up approach can provide insight into how communities change under stress.
Temperature is among the cardinal environmental variables which determine the composition and function of microbial communities. Many culture-independent studies have characterized communities that are affected by changing temperatures, either due to seasonal cycles 1-3 , long-term warming 4-6 , or latitudinal/elevational gradients 7-8. However, a predictive understanding of how microbial communities respond to such changes in temperature is still lacking, partly because it is not obvious which aspects of microbial physiology determine whether a species should benefit from temperature alteration. Here, we incorporate how microbial growth rates change with temperature to a modified Lotka-Volterra competition model 9 , and predict that higher temperatures should generically favor slower-growing species in a bacterial community. We experimentally confirm this prediction in pairwise cocultures assembled from a diverse set of species, and we show that these changes to pairwise outcomes with temperature are also predictive of changing outcomes in three-species communities, suggesting our theory may propagate 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 bridge the gap between ecological theory and the complex dynamics observed in metagenomic surveys. Experimental microbial communities are normally incubated at a fixed temperature. We aimed to determine how changing this incubation temperature would affect the outcome of a microbial coculture in which the two species were known to stably coexist at our usual experimental temperature of 25°C. We focused on two naturally co-occurring species isolated from soil (Aci1 and Pan1), and followed a standard coculture methodology (see Methods) at three experimental temperatures: 16°C, 25°C, and 30°C. At each of these three temperatures, Aci1 is the faster growing species, and the difference in the growth rates of the two species increases alongside temperature (Figure 1A). Accordingly, we assumed that the slower-growing Pan1 would be favored by lowering the temperature and disfavored by raising the temperature, as its competitive ability would likely be hindered by a larger disparity in growth rate. Surprisingly, we observed the opposite, and found that Pan1 in fact becomes a stronger competitor at higher temperature, with the coculture outcome shifting from Aci1 dominance at 16°C (Figure 1B) to coexistence at 25°C (Figure 1C) and finally to Pan1 dominance at 30°C (Figure 1D).
The effect of environmental fluctuations is a major question in ecology. While it is widely accepted that fluctuations and other types of disturbances can increase biodiversity, there are fewer examples of other types of outcomes in a fluctuating environment. Here we explore this question with laboratory microcosms, using cocultures of two bacterial species, P. putida and P. veronii. At low dilution rates we observe competitive exclusion of P. veronii, whereas at high dilution rates we observe competitive exclusion of P. putida. When the dilution rate alternates between high and low, we do not observe coexistence between the species, but rather alternative stable states, in which only one species survives and initial species' fractions determine the identity of the surviving species. The Lotka-Volterra model with a fluctuating mortality rate predicts that this outcome is independent of the timing of the fluctuations, and that the time-averaged mortality would also lead to alternative stable states, a prediction that we confirm experimentally. Other pairs of species can coexist in a fluctuating environment, and again consistent with the model we observe coexistence in the time-averaged dilution rate. We find a similar time-averaging result holds in a three-species community, highlighting that simple linear models can in some cases provide powerful insight into how communities will respond to environmental fluctuations.
6All organisms are sensitive to the abiotic environment, and a deteriorating 7 environment can lead to extinction. However, survival in a multispecies 8 community also depends upon inter-species interactions, and some species may 9 even be favored by a harsh environment that impairs competitors. A 10 deteriorating environment can thus cause surprising transitions in community 11 composition. Here, we combine theory and laboratory microcosms to develop a 12 predictive understanding of how simple multispecies communities change under 13 added mortality, a parameter that represents environmental harshness. In order 14to explain changes in a multispecies microbial system across a mortality gradient, 15we examine its members' pairwise interactions. We find that increasing mortality 16 favors the faster grower, confirming a prediction of simple models. Furthermore, 17if the slower grower outcompetes the faster grower in environments with low or 18 no added mortality, the competitive outcome can reverse as mortality increases. 19We find that this tradeoff between growth rate and competitive ability is indeed 20 prevalent in our system, allowing for striking pairwise outcome changes that 21 propagate up to multispecies communities. These results argue that a bottom-up 22 approach can provide insight into how communities will change under stress. 23
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