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Chemical Ecology of the Marine Actinomycete Genus Salinispora

Abstract

Chemical ecology is a rich field of study that addresses how organisms communicate and compete using small organic molecules. In bacteria, much of what is known comes from natural products discovery research. The isolation of thousands of pharmaceutically relevant small molecules like antibiotics, as well as more recent genomic work showing the potential for many more yet to be discovered, has provided an important knowledge base of bacterial chemical diversity. However, the vast majority of these natural products have unknown ecological functions. Compounds produced by marine bacteria are particularly poorly understood due to a relative lack of study on the microbial ecosystem dynamics. This dissertation consists of five chapters that address questions of ecology in relation to the bioactive molecules produced by the marine actinomycete genus Salinispora. The first chapter introduces the topic of chemical ecology and microbial secondary metabolites, followed by three data chapters and a summary chapter.

Chapter 2 presents the results of a study on the differences in antagonism between the two species S. arenicola and S. tropica. The greater levels of inhibition by S. arenicola, combined with its slower growth rate and reduced ability to access iron, provide evidence that this species employs interference competition as a strategy while S. tropica is characterized by exploitative competition. The two closely related species exist in a microdiverse cluster, supporting the idea that fine-scale differentiation can occur in bacteria that are otherwise closely related.

Chapter 3 examines the antibiotic activities of S. tropica, a species not previously known to produce antibiotics. More specifically, it assesses the role of co-culturing S. tropica with other bacterial strains in inducing compound production. These experiments provide a nuanced picture of compound up regulation with respect to a specific challenger as opposed to general nutrient depletion, which can also occur in a monoculture over time. It provides new insight into the dynamics of microbial interactions and offers potential candidate molecules and masses for future studies on antibiotic activity.

After narrowing the focus to individual interactions in Chapter 3, Chapter 4 expands outwards for a broader perspective by examining the effects of Salinispora arenicola secondary metabolites on sediment microbial communities. Using a mesocosm experimental design and high-throughput amplicon sequencing, community composition was assessed before and after treatment with S. arenicola culture extracts. There were consistent shifts in composition, with several taxa significantly depleted including predatory bacteria like Saprospira spp. and Bdellovibrio spp. Lab experiments largely supported the culture-independent results seen in the mesocosms. This study is the first of its kind to assess community-wide effects of marine actinomycete secondary metabolites and provides valuable insight into the ecological dynamics of these environments.

Chapter 5 offers some concluding thoughts on the place of this dissertation in the field of chemical ecology. It also provides some outlook on the current and future state of research in this field.

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