PMID- 31180327 OWN - NLM STAT- MEDLINE DCOM- 20200302 LR - 20240418 IS - 2050-084X (Electronic) IS - 2050-084X (Linking) VI - 8 DP - 2019 Jun 10 TI - Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations. LID - 10.7554/eLife.45084 [doi] LID - e45084 AB - 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. CI - (c) 2019, Armbruster et al. FAU - Armbruster, Catherine R AU - Armbruster CR AUID- ORCID: 0000-0003-0795-802X AD - Department of Microbiology, University of Washington, Seattle, United States. FAU - Lee, Calvin K AU - Lee CK AUID- ORCID: 0000-0001-6789-0317 AD - Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States. AD - Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, United States. AD - California NanoSystems Institute, University of California, Los Angeles, Los Angeles, United States. FAU - Parker-Gilham, Jessica AU - Parker-Gilham J AD - Department of Microbiology, University of Washington, Seattle, United States. FAU - de Anda, Jaime AU - de Anda J AD - Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States. AD - Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, United States. AD - California NanoSystems Institute, University of California, Los Angeles, Los Angeles, United States. FAU - Xia, Aiguo AU - Xia A AD - Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China. FAU - Zhao, Kun AU - Zhao K AD - Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, China. AD - Collaborative Innovation Centre of Chemical Science and Engineering, Tianjin University, Tianjin, China. FAU - Murakami, Keiji AU - Murakami K AD - Department of Oral Microbiology, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, Japan. FAU - Tseng, Boo Shan AU - Tseng BS AUID- ORCID: 0000-0001-7563-0232 AD - School of Life Sciences, University of Nevada, Las Vegas, United States. FAU - Hoffman, Lucas R AU - Hoffman LR AD - Department of Microbiology, University of Washington, Seattle, United States. AD - Department of Pediatrics, University of Washington, Seattle, United States. FAU - Jin, Fan AU - Jin F AUID- ORCID: 0000-0003-2313-0388 AD - Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China. AD - Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China. FAU - Harwood, Caroline S AU - Harwood CS AD - Department of Microbiology, University of Washington, Seattle, United States. FAU - Wong, Gerard Cl AU - Wong GC AD - Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States. AD - Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, United States. AD - California NanoSystems Institute, University of California, Los Angeles, Los Angeles, United States. FAU - Parsek, Matthew R AU - Parsek MR AUID- ORCID: 0000-0003-2932-7966 AD - Department of Microbiology, University of Washington, Seattle, United States. AD - Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, China. LA - eng GR - K24HL141669/NH/NIH HHS/United States GR - K22AI121097/NH/NIH HHS/United States GR - GM56665/GM/NIGMS NIH HHS/United States GR - T32 GM007270/GM/NIGMS NIH HHS/United States GR - R01 AI077628/AI/NIAID NIH HHS/United States GR - T32GM007270/NH/NIH HHS/United States GR - K24 HL141669/HL/NHLBI NIH HHS/United States GR - 1R01AI143730-01/NH/NIH HHS/United States GR - R01 AI143916/AI/NIAID NIH HHS/United States GR - R01 GM056665/GM/NIGMS NIH HHS/United States GR - 5R01AI077628/NH/NIH HHS/United States GR - R01AI143916/NH/NIH HHS/United States GR - R01 AI134895/AI/NIAID NIH HHS/United States GR - K22 AI121097/AI/NIAID NIH HHS/United States GR - R01 AI143730/AI/NIAID NIH HHS/United States PT - Journal Article PT - Research Support, N.I.H., Extramural PT - Research Support, Non-U.S. Gov't PT - Research Support, U.S. Gov't, Non-P.H.S. DEP - 20190610 PL - England TA - Elife JT - eLife JID - 101579614 RN - 0 (Bacterial Proteins) RN - 61093-23-0 (bis(3',5')-cyclic diguanylic acid) RN - H2D2X058MU (Cyclic GMP) SB - IM EIN - Elife. 2020 May 26;9:. PMID: 32452764 MH - Bacterial Adhesion/genetics/physiology MH - Bacterial Proteins/genetics/*metabolism MH - Biofilms/growth & development MH - Cell Membrane/*metabolism MH - Cyclic GMP/*analogs & derivatives/metabolism MH - Gene Expression Regulation, Bacterial MH - Pseudomonas aeruginosa/genetics/*metabolism/physiology MH - Quorum Sensing/genetics PMC - PMC6615863 OAB - Bacteria can adopt different lifestyles, depending on the environment in which they grow. They can exist as single cells that are free to explore their environment or group together to form 'biofilms'. The bacteria in biofilms stick to a surface, and produce a slimy 'matrix' that covers and thereby protects them. Biofilms have been found in lung infections that affect people with the genetic disorder cystic fibrosis, and can also form on the surface of medical implants. Because the biofilm lifestyle protects bacteria from the immune system and antimicrobial drugs, learning about how biofilms form could help researchers to discover ways to prevent and treat such infections. Many bacteria switch between the free-living and biofilm lifestyles by altering their levels of a signaling molecule called cyclic diguanylate monophosphate (called c-di-GMP for short). Bacteria living in biofilms have much higher levels of c-di-GMP than their free-living counterparts, and bacteria that have high levels of c-di-GMP produce more biofilm matrix. Bacteria called Pseudomonas aeruginosa use a protein signaling complex called the Wsp system to sense that they are on a surface and increase c-di-GMP production. Questions remained about how quickly this change in production occurs, and whether bacteria pass on their c-di-GMP levels to the new descendant cells when they divide. Armbruster et al. monitored individual cells of P. aeruginosa producing c-di-GMP as they began to form biofilms. Unexpectedly, not all cells increased their c-di-GMP levels when they first attached to a surface. Instead, Armbruster et al. found that there are two populations - high and low c-di-GMP cells - that each perform complementary and important tasks in the early stages of biofilm formation. The high c-di-GMP cells represent 'biofilm founders' that start to produce the biofilm matrix, whereas the low c-di-GMP cells represent 'surface explorers' that spend more time traveling along the surface. Armbruster et al. found that the Wsp surface sensing system generates these two populations of cells. Moreover, the c-di-GMP levels in a bacterial cell even affect the behavior of the descendant cells that form when it divides. This effect can persist for several cell generations. More work is needed to examine exactly how the biofilm founders and surface explorers interact and influence how biofilms form, and to discover if blocking c-di-GMP signaling prevents biofilm formation. This could ultimately lead to new strategies to prevent and treat infections in humans. OABL- eng OTO - NOTNLM OT - Pseudomonas aeruginosa OT - Wsp system OT - biofilm OT - c-di-gmp OT - infectious disease OT - microbiology OT - surface sensing COIS- CA, CL, JP, Jd, AX, KZ, BT, LH, FJ, CH, GW, MP No competing interests declared EDAT- 2019/06/11 06:00 MHDA- 2020/03/03 06:00 PMCR- 2019/06/10 CRDT- 2019/06/11 06:00 PHST- 2019/01/11 00:00 [received] PHST- 2019/06/08 00:00 [accepted] PHST- 2019/06/11 06:00 [pubmed] PHST- 2020/03/03 06:00 [medline] PHST- 2019/06/11 06:00 [entrez] PHST- 2019/06/10 00:00 [pmc-release] AID - 45084 [pii] AID - 10.7554/eLife.45084 [doi] PST - epublish SO - Elife. 2019 Jun 10;8:e45084. doi: 10.7554/eLife.45084.