Regulatory protein HilD stimulates Salmonella Typhimurium invasiveness by promoting smooth swimming via the methyl-accepting chemotaxis protein McpC

• Published in: Nature communications Vol. 12; no. 1; p. 348
• Main Authors: Cooper, Kendal G., Chong, Audrey, Kari, Laszlo, Jeffrey, Brendan, Starr, Tregei, Martens, Craig, McClurg, Molly, Posada, Victoria R., Laughlin, Richard C., Whitfield-Cargile, Canaan, Garry Adams, L., Bryan, Laura K., Little, Sara V., Krath, Mary, Lawhon, Sara D., Steele-Mortimer, Olivia
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 13.01.2021; Nature Publishing Group; Nature Portfolio
• Subjects: 13/1; 13/106; 13/51; 14/19; 14/63; 38; 38/35; 38/39; 38/70; 42; 45; 45/29; 45/77; 631/326/41/2531; 631/326/41/88; 631/326/421; 64; 82/51; Animals; Arrays; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Caco-2 Cells; Cattle; Cells, Cultured; Chemotaxis; Chemotaxis - genetics; Chemotaxis - physiology; Epithelial cells; Flagella; Gene Expression Regulation, Bacterial; Genes; HeLa Cells; Humanities and Social Sciences; Humans; Invasiveness; Ligands; Methyl-Accepting Chemotaxis Proteins - genetics; Methyl-Accepting Chemotaxis Proteins - metabolism; Mice; Mice, Inbred C57BL; Motility; Movement - physiology; multidisciplinary; Mutation; Protein arrays; Proteins; Receptors; Salmonella; Salmonella Infections - microbiology; Salmonella Typhimurium; Salmonella typhimurium - genetics; Salmonella typhimurium - metabolism; Salmonella typhimurium - physiology; Science; Science (multidisciplinary); Secretion; Swimming; Swimming behavior; Transcription Factors - genetics; Transcription Factors - metabolism; Tumbling
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-20558-6

In the enteric pathogen Salmonella enterica serovar Typhimurium, invasion and motility are coordinated by the master regulator HilD, which induces expression of the type III secretion system 1 (T3SS1) and motility genes. Methyl-accepting chemotaxis proteins (MCPs) detect specific ligands and control the direction of the flagellar motor, promoting tumbling and changes in direction (if a repellent is detected) or smooth swimming (in the presence of an attractant). Here, we show that HilD induces smooth swimming by upregulating an uncharacterized MCP (McpC), and this is important for invasion of epithelial cells. Remarkably, in vitro assays show that McpC can suppress tumbling and increase smooth swimming in the absence of exogenous ligands. Expression of mcpC is repressed by the universal regulator H-NS, which can be displaced by HilD. Our results highlight the importance of smooth swimming for Salmonella Typhimurium invasiveness and indicate that McpC can act via a ligand-independent mechanism when incorporated into the chemotactic receptor array. Protein HilD of Salmonella Typhimurium coordinates motility and host cell invasion by upregulating flagellar genes and a secretion system. Here, Cooper et al. show that HilD also modulates swimming behaviour by upregulating a subunit of the chemotactic receptor array, and this is important for invasion of epithelial cells.