Metabolic adaptation to consume butyrate under prolonged resource exhaustion

• Published in: PLoS genetics Vol. 19; no. 6; p. e1010812
• Main Authors: Katz, Sophia, Grajeda-Iglesias, Claudia, Agranovich, Bella, Ghrayeb, Alia, Abramovich, Ifat, Hilau, Sabrin, Gottlieb, Eyal, Hershberg, Ruth
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 22-06-2023; Public Library of Science (PLoS)
• Subjects: Amino acids; Analysis; Bacteria; Biology and Life Sciences; Escherichia coli; Esters; Fatty acids; Gene mutations; Genetic aspects; Identification and classification; Medicine and Health Sciences; Properties; Research and Analysis Methods; Soil productivity; Sweden
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1010812

Bacteria must often survive following the exhaustion of their external growth resources. Fitting with this need, many bacterial species that cannot sporulate, can enter a state known as long term stationary phase (LTSP) in which they can persist for years within spent media. Several recent studies have revealed the dynamics of genetic adaptation of Escherichia coli under LTSP. Yet, the metabolic consequences of such genetic adaptation were not addressed. Here, we characterized the metabolic changes LTSP populations experience, over the first 32 days under LTSP. This allowed us to link genetic adaptations observed in a convergent manner across LTSP populations back to their metabolic adaptive effect. Specifically, we demonstrate that through the acquisition of mutations combinations in specific sets of metabolic genes, E. coli acquires the ability to consume the short chain fatty acid butyrate. Intriguingly, this fatty acid is not initially present within the rich media we used in this study. Instead, it is E. coli itself that produces butyrate during its initial growth within fresh rich media. The mutations that enable butyrate consumption allow E. coli to grow on butyrate. However, the clones carrying these mutations rapidly decrease in frequency, once the butyrate is consumed, likely reflecting an associated cost to fitness. Yet despite this, E. coli populations show a remarkable capability of maintaining these genotypes at low frequency, as standing variation. This in turn allows them to more rapidly re-adapt to consume butyrate, once it again becomes available to them.