Altruistic feeding and cell-cell signaling during bacterial differentiation actively enhance phenotypic heterogeneity
Starvation triggers bacterial spore formation, a committed differentiation program that transforms a vegetative cell into a dormant spore. Cells in a population enter sporulation nonuniformly to secure against the possibility that favorable growth conditions, which put sporulation-committed cells at a disadvantage, may resume. This heterogeneous behavior is initiated by a passive mechanism: stochastic activation of a master transcriptional regulator. Here, we identify a cell-cell communication pathway containing the proteins ShfA (YabQ) and ShfP (YvnB) that actively promotes phenotypic heterogeneity, wherein <i>Bacillus subtilis</i> cells that start sporulating early use a calcineurin-like phosphoesterase to release glycerol, which simultaneously acts as a signaling molecule and a nutrient to delay nonsporulating cells from entering sporulation. This produced a more diverse population that was better poised to exploit a sudden influx of nutrients compared to those generating heterogeneity via stochastic gene expression alone. Although conflict systems are prevalent among microbes, genetically encoded cooperative behavior in unicellular organisms can evidently also boost inclusive fitness.
Authors
- Lisa M. Miller Jenkins (ORCID: https://orcid.org/0000-0003-1245-1338)
- Thomas Nipper (ORCID: https://orcid.org/0000-0002-5307-2927)
- Vivek Anantharaman (ORCID: https://orcid.org/0000-0001-8395-0009)
- L. Aravind (ORCID: https://orcid.org/0000-0003-0771-253X)
- Jiji Chen (ORCID: https://orcid.org/0000-0002-4426-3035)
- Hyo Moon Cho (ORCID: https://orcid.org/0000-0003-3447-8726)
- Hari Shroff (ORCID: https://orcid.org/0000-0003-3613-8215)
- Carissa Chan (ORCID: https://orcid.org/0000-0003-3054-0879)
- Yijun Su (ORCID: https://orcid.org/0009-0001-4630-7863)
- Hyoyoung Choo‐Wosoba (ORCID: https://orcid.org/0000-0002-8756-1016)
- Taylor B. Updegrove (ORCID: https://orcid.org/0000-0002-9763-3618)
- Thomas Delerue (ORCID: https://orcid.org/0000-0002-8900-247X)
- Kumaran S. Ramamurthi (ORCID: https://orcid.org/0000-0002-2335-3568)
- Carole A. Bewley (ORCID: https://orcid.org/0000-0003-2203-0852)
- Lixia Zhang (ORCID: https://orcid.org/0000-0001-8259-9552)
Institutions
- National Institutes of Health (US)
- Howard Hughes Medical Institute (US)
- Janelia Research Campus (US)
- National Institute of Biomedical Imaging and Bioengineering (US)
- National Institute of Diabetes and Digestive and Kidney Diseases (US)
- Office of the Director (US)
- National Cancer Institute (US)
Publication Details
- Journal
- Science Advances
- Published
- 2024-10-18
- DOI
- https://doi.org/10.1126/sciadv.adq0791
- Citations
- 4
- Primary Topic
- Bacterial Genetics and Biotechnology
- Type
- article
- Field-Weighted Citation Impact
- 2.20
Funders
- National Institutes of Health
- National Cancer Institute
- National Institute of Diabetes and Digestive and Kidney Diseases
- U.S. National Library of Medicine