Bioactive exometabolites drive maintenance competition in simple bacterial communities

Abstract

During prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced by cells in stationary phase cultures, can, perhaps counterintuitively, include upregulation of cellular secondary metabolism and release of exometabolites into the local environment, at the cost of an energetic commitment to growth. As resource limitation is a characteristic feature of many habitats that harbor environmental microbial communities, we hypothesized that neighboring bacterial populations employ exometabolites to compete or cooperate during maintenance, and that these exometabolite-facilitated interactions can drive community outcomes. Here, we evaluated the consequences of exometabolite interactions over stationary phase among three well-known environmental bacterial strains: Burkholderia thailandensis E264 (ATCC 700388), Chromobacterium violaceum ATCC 31532, and Pseudomonas syringae pv.tomato DC3000 (ATCC BAA-871). We assembled these stains into laboratory-scale synthetic communities that only permitted chemical interactions among them. We compared the responses (transcripts) and behaviors (exometabolites) of each member with and without neighbors. We found that transcriptional dynamics were altered in the presence of different neighbors, and that these changes could be attributed to the production of or response to bioactive exometabolites employed for competition during maintenance. B. thailandensis was especially influential and competitive within its communities, as it consistently upregulated additional biosynthetic gene clusters involved in the production of bioactive exometabolites for both exploitative and interference competition. Additionally, some of these bioactive exometabolites were upregulated and produced in a non-additive manner in the 3-member community. These results demonstrate that the active investment in competition during maintenance can contribute to both bacterial population fitness and community-level outcomes. It also suggests that the traditional concept of defining competitiveness by growth outcomes may be too narrow, and that maintenance competition could be an alternative measure.