Ecology and evolution of synergy and antagonism among microbes

Abstract

Humans have long shown interest in understanding relationships between organisms and scientists have long investigated how organismal interactions are structured and evolve, including conspecific interactions within and between social groups and interactions between species. Biological communities are made up of a variety of interacting individuals, from large animals to tiny microorganisms, all of which are connected in one way or another. Bacteria, however, form the foundation of nearly all ecosystems, and knowing how they interact in the face of constant abiotic and biotic perturbances is crucial to understanding their population dynamics, their diversification and evolutionary history. The aim of this thesis is to better understand the importance of beneficial and antagonistic interactions and how they shape the ecology and evolution of bacterial populations. More specifically, it focuses on the effect that different levels of intergroup migration can have on within-group interactions and on how bacteria-phage interactions evolve. To address these topics, Myxococcus xanthus was used as a model system. The social bacterium M. xanthus is commonly found in soil communities and performs a variety of social behaviors, ranging from cooperative swarming and predation to the formation of multicellular fruiting bodies that harbor stress resistant spores that germinate in a cooperative manner. A unique social life cycle and interactions with many other organisms, such as prey or bacteriophages, make M. xanthus an attractive study organism for understanding the evolution of social behavior. First, we investigated how different levels of migration between groups of M. xanthus affect group-level performance and the resulting dynamics within groups (Chapter 1). Using populations that evolved under either low levels of intergroup migration or regular intergroup mixing, we show that group-level performance is higher when evolved under low levels of migration, as a result of reduced intragroup conflict. The focus of Chapter 1 is on intraspecific interactions. We see how limitation of intergroup migration during evolution can have a major influence on the evolution of cooperation in bacteria. In Chapter 2, we ask whether how evolution in populations engaging in cooperative intraspecific interactions affects subsequent interspecific interactions, using the example of antagonistic interactions between M. xanthus and the virulent phage Mx1. Specifically, we investigated how evolution by M. xanthus in the absence of phage and under high selective pressure on intraspecific cooperation behaviors, such as cooperative motility, later affects interspecific interaction with phage (Chapter 2). We show that evolution in the absence of phage can lead to increased host resistance. Diversification in susceptibility to phage among evolved populations was not primarily caused by differences in the selective environments experienced by evolving bacteria, but rather by variation in random mutational input. The character of direct interactions between natural isolates of M. xanthus and phage Mx1 are the topic of Chapter 3. Bacteria-phage interactions are commonly looked at from the antagonistic perspective of the phage towards the bacterial cell. Here, we have identified apparent anti-phage defense mechanisms mainly in the form of diffusible extracellular compounds released by M. xanthus cells that harm free phage particles. The ability of bacterial cells to fight phage threats prior to infection may represent a previously unknown form of protection. These results highlight the complexity and importance of interaction effects for the evolution of biological diversity and social evolution, and how latent effects can play important roles alongside immediate responses to direct interactions.