Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States; Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, United States; California NanoSystems Institute, University of California, Los Angeles, Los Angeles, United States
Jessica Parker-Gilham
Department of Microbiology, University of Washington, Seattle, United States
Jaime de Anda
Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States; Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, United States; California NanoSystems Institute, University of California, Los Angeles, Los Angeles, United States
Aiguo Xia
Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China
Kun Zhao
Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, China; Collaborative Innovation Centre of Chemical Science and Engineering, Tianjin University, Tianjin, China
Keiji Murakami
Department of Oral Microbiology, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, Japan
School of Life Sciences, University of Nevada, Las Vegas, United States
Lucas R Hoffman
Department of Microbiology, University of Washington, Seattle, United States; Department of Pediatrics, University of Washington, Seattle, United States
Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China; Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China
Caroline S Harwood
Department of Microbiology, University of Washington, Seattle, United States
Gerard CL Wong
Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States; Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, United States; California NanoSystems Institute, University of California, Los Angeles, Los Angeles, United States
Department of Microbiology, University of Washington, Seattle, United States; Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, China
The second messenger signaling molecule cyclic diguanylate monophosphate (c-di-GMP) drives the transition between planktonic and biofilm growth in many bacterial species. Pseudomonas aeruginosa has two surface sensing systems that produce c-di-GMP in response to surface adherence. Current thinking in the field is that once cells attach to a surface, they uniformly respond by producing c-di-GMP. Here, we describe how the Wsp system generates heterogeneity in surface sensing, resulting in two physiologically distinct subpopulations of cells. One subpopulation has elevated c-di-GMP and produces biofilm matrix, serving as the founders of initial microcolonies. The other subpopulation has low c-di-GMP and engages in surface motility, allowing for exploration of the surface. We also show that this heterogeneity strongly correlates to surface behavior for descendent cells. Together, our results suggest that after surface attachment, P. aeruginosa engages in a division of labor that persists across generations, accelerating early biofilm formation and surface exploration.
