Manipulating the strength of organism–environment feedback increases nonlinearity and apparent hysteresis of ecosystem response to environmental change

Theory predicts that organism–environment feedbacks play a central role in how ecological communities respond to environmental change. Strong feedback causes greater nonlinearity between environmental change and ecosystem state, increases the likelihood of hysteresis in response to environmental change, and augments the possibility of alternative stable regimes. To illustrate these predictions and their dependence on a temporal scale, we simulated a minimal ecosystem model. To test the predictions, we manipulated the feedback strength between the metabolism and the dissolved oxygen concentration in an aquatic heterotrophic tri‐trophic community in microecosystems. The manipulation consisted of five levels, ranging from low to high feedback strength by altering the oxygen diffusivity: free gas exchange between the microcosm atmosphere and the external air (metabolism not strongly affecting environmental oxygen), with the regular addition of 200, 100, or 50 ml of air and no gas exchange. To test for nonlinearity and hysteresis in response to environmental change, all microecosystems experienced a gradual temperature increase from 15 to 25°C and then back to 15°C. We regularly measured the dissolved oxygen concentration, total biomass, and species abundance. Nonlinearity and hysteresis were higher in treatments with stronger organism–environment feedbacks. There was no evidence that stronger feedback increased the number of observed ecosystem states. These empirical results are in broad agreement with the theory that stronger feedback increases nonlinearity and hysteresis. They therefore represent one of the first direct empirical tests of the importance of feedback strength. However, we discuss several limitations of the study, which weaken confidence in this interpretation. Research demonstrating the causal effects of feedback strength on ecosystem responses to environmental change should be placed at the core of efforts to plan for sustainable ecosystems

Bistable dynamics in microbial ecology and systems biology

Bistability, in which a system has two stable states, is a common property of many dynamic systems. This thesis explores the properties of such systems across a range of length scales, from gene circuits to ecosystems. Cells often store memories of environmental stimuli using bistable gene circuits. High fidelity memory storage requires that a state has a long lifetime. However, an underappreciated aspect of stable memory is that the distance from a bifurcation could determine how sensitive a state is to perturbations in the extracellular environment. We predict that cell memory should become increasingly sensitive to perturbations near a bifurcation and test this idea in three different gene circuits: a toggle switch, the yeast galactose utilization network, and the E. coli lactose utilization network. In a second study, we explore how the environmental context in which two species interact can influence their mode of interaction. Two species in nature often form reciprocally beneficial partnerships termed mutualisms, but in certain environmental regimes the species might shift to competing with one another for resources. This mutualism-competition transition has been understudied in experimental ecosystems. Using a synthetic yeast cross-feeding mutualism, we modulate the degree to which two partners rely on each other by supplementing the cells with variable amounts of nutrients. Surprisingly, we find that as the amount of supplemented nutrients is increased, the system passes through eight qualitatively distinct dynamic regimes: extinction, obligatory mutualism, obligatory/facultative mutualism, facultative mutualism, parasitism, amensalism, competition, and competitive exclusion. In a third study, we probe how population growth dynamics can influence the probability of evolutionary rescue. Natural populations frequently face harsh environments in which their death rate exceeds their birth rate and population size tends toward zero. In such scenarios, populations can either go extinct, migrate to a better habitat, or adapt to the harsh environment. Natural populations often exhibit an “Allee effect,” in which populations grow slowly at low density due to struggles with such behaviors as finding a mate or collective hunting. We hypothesize that the presence of an Allee effect could impede evolutionary rescue and confirm this hypothesis in a model laboratory yeast ecosystem.Biophysic

A single-cell view on the intra- and inter-population metabolic heterogeneity and ecophysiology of microorganisms at different ecological scales

Metabolic heterogeneity (MH) occurs when isogenic microbial populations display cell-to-cell differences in metabolic traits, albeit exposed to homogeneous conditions. Despite the increasing focus on MH, its triggering factors remain largely unknown. In the present thesis, I used stable isotope probing and chemical imaging with nanoscale Secondary Ion Mass Spectrometry (nanoSIMS) to study MH at single-cell level, in model organisms, synthetic and natural communities, to understand i) how abiotic factors, biotic interactions and antibiotics exposure influence MH and ii) its potential ecological role. Moreover, I optimized sample preparation for chemical and high-resolution imaging and suggested two different indices as ‘unit measure’ of MH. As results, I have shown for the first time that MH is displayed by microorganisms under favorable growth conditions, although none of the tested abiotic factors prevailed as the main trigger of MH. I brought insights on how biotic interactions play a role in the functional heterogeneity using bacteria pseudo-fungi co-cultures. I found that antibiotics reduce Carbon and Nitrogen assimilation rates of targeted phylogenetic groups in river-water communities, while increasing their MH, pointing to its ecological importance in natural environments. To conclude, I provided novel insights on the phenomenon of MH and its dynamics at different ecological scales.:Abbreviation list Summary Introduction Knowledge gaps Results and discussion - Optimization of sample preparation - Validation of quantitation methods - Abiotic factors shaping metabolic heterogeneity in bacterial populations - Influence of biotic factors in shaping heterogeneity - Metabolic Heterogeneity and ecophysiology of natural microbial populations influenced by emerging contaminants Conclusions Outlook Bibliography Appendix Acknowledgments Curriculum Vitae List of publication

The Role of Quorum Sensing in Bacterial Colony Dynamics

The quorum sensing (QS) signalling system allows colonies of bacteria to coordinate gene expression to optimise behaviour at low and high cell densities, giving rise to individual and group responses, respectively. The main aim of this thesis is to understand better the important roles of QS in bacterial colony dynamics. Thus a mathematical description was developed to thoroughly explore key mechanisms and parameter sensitivity. The nature of the QS system depends very much on the species. Pseudomonas aeruginosa was chosen as a model species for this study. P. aeruginosa is a Gram-negative bacterium that is responsible for a wide range of chronic infections in humans. Its QS signalling system is known to involve the las, rhl and pqs systems; this thesis focuses on the first two. The las system includes the LasR regulator and LasI synthase, which direct the synthesis of autoinducer 3O-C12-HSL. Similarly, the rhl system consists of the RhlR regulator and RhlI synthase, directing the synthesis of autoinducer C4-HSL. The mathematical model of the las system displays hysteresis phenomena and excitable dynamics. In essence, the system can have two stable steady states reflecting low and high signal molecule production, separated by one unstable steady state. This feature of the las system can give rise to excitable pulse generation with important downstream impact on the rhl system. The las system is coupled to the rhl system in two ways. First, LasR and 3O-C12-HSL activate the expression of their counterpart in the rhl system. Second, 3O-C12-HSL blocks activation of RhlR by C4-HSL. Furthermore, the las-rhl interaction provides a `quorum memory' that allows cells to trigger rhamnolipid production when they are at the edge of colony. It was demonstrated how the dynamical QS system in individual cells and with coupling between cells can affect the dynamics of the bacterial colony