Membrane fluidity optimization regulates Serratia marcescens swarming behaviour through modulation of a temperature-dependent two-component signal transduction system

Serratia marcescens swarming behavior is characterized by continuous populational surface migration on swarming agar at 30°C, but not at 37°C. The underlying mechanism how S. marcescens population starts to initiate swarming and the temperature-dependent regulation of swarming behaviour are currently uncharacterized. We identify in S. marcescens a genetic locus that, when mutated, results in a ”super-swarming” phenotype, which is not only defective in the temporal, but also in the temperature-dependent control of swarming behaviours. The gene mutated (rssA, Regulation of Serratia Swarming A) is homologous to membrane sensor histidine kinases of the two-component family of regulatory proteins, suggesting that RssA may function as a sensor of environmental conditions required to regulate swarming migration. Factors already identified to be involved in regulation of swarming migration are not affected in this mutant. These include amount of flagellum synthesis, activity of swimming motility, surfactant production, and synthesis of extracellular polysaccharide. Here we report that long chain fatty acids and temperature shift acting as the signal cues regulate S. marcescens CH-1 swarming through the RssA/RssB two component signal transduction system. We find that long chain fatty acids and temperature upshift negatively regulate the CH-1 swarming through influencing pattern of cellular fatty acid profile. The RssA-RssB two-component system mediates this response, as both partners are required to sense and transduce the signals. Fatty acid profile analysis strongly indicates that long chain fatty acid and temperature affects the signaling state of the RssA sensor protein by increasing the incorporation of the low0melting point fatty acids into membrane phospholipid. We propose that both increase in membrane fluidity at constant temperature and a temperature upshift influences fatty acid synthesis and swarming by the same mechanism. Similar phenomena of long chain fatty acid inhibition were also observed in swarming regulation of Proteus mirabilis and Salmonella typhimurium. Thus, the fatty acid profile and two component signaling pathway might provide a novel and common mechanism for regulation of swarming behaviour of not only S. marcescens, but also other swarming bacteria under different physiological culture conditions.