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Community-specific cell death sustains bacterial expansion under phosphorus starvation

Nature Chemical Biology volume 21, pages 867–875 (2025)Cite this article

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Abstract

Colony expansion is important for establishing territories. It is unclear to what extent bacteria can maintain colony expansion under nutrient limitation. Here, we found that Escherichia coli biofilms could maintain steady expansion for an extended period of time under severe phosphorus limitation. The expansion was supported by reactive-oxygen-species-mediated cell death within the biofilm. The cell death was spatially separated from the region of growth, resulting in cross-regional recycling of phosphorus from the lysed bacteria. The increase in cell death and the steady growth after phosphorus removal was community specific and was not observed in planktonic bacteria. Lastly, phosphorus had a unique role in the cell-death-mediated nutrient recycling, as the phenomenon described above was not observed under carbon or nitrogen starvation. Our work reveals how bacterial communities use spatially coordinated metabolism to cope with phosphorus limitation, which promotes robust expansion of the bacteria in fluctuating environments.

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Fig. 1: Expansion of E. coli biofilm.
Fig. 2: Phosphorus in the extracellular environment of the biofilm.
Fig. 3: Cell death in the biofilm after phosphorus removal.
Fig. 4: ROS in the biofilm after phosphate removal.
Fig. 5: Death and expansion after phosphate removal is biofilm and phosphorus specific.
Fig. 6: Scheme describing bacterial response to the removal of different nutrients.

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Acknowledgements

We thank L. Ma, M. Asally, Y. Wang and members of the J.L. lab for helpful discussions. We thank the Tsinghua University Center of Pharmaceutical Technology for assistance on the metabolomics experiments. J.L. was supported by the National Key R&D Program of China (2023YFC2306300), the National Natural Science Foundation of China (32170099), the Tsinghua University Dushi Program (20221080020 and 20231080040) and the Tsinghua–Peking Center for Life Sciences.

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  1. These authors contributed equally: Ziyan Wang, Lingbin Zeng, Shouxian Hu.

Authors and Affiliations

  1. Center for Infection Biology, School of Basic Medical Sciences, Tsinghua University, Beijing, China

    Ziyan Wang, Lingbin Zeng, Shouxian Hu, Qianyu Hu, Yuzhen Zhang & Jintao Liu

  2. Tsinghua–Peking Center for Life Sciences, Beijing, China

    Yuzhen Zhang & Jintao Liu

  3. SXMU–Tsinghua Collaborative Innovation Center for Frontier Medicine, Shanxi Medical University, Taiyuan, China

    Jintao Liu

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Contributions

Z.W. and J.L. designed the research. Z.W., L.Z. and S.H. performed the experiments for the initial submission. Z.W., S.H. and Q.H. performed the experiments for the revision. Z.W., S.H., L.Z. and J.L. analyzed the data. Y.Z. assisted with making the microfluidic chip during the early stage of the project. Z.W. and J.L. wrote the manuscript.

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Correspondence to Jintao Liu.

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Nature Chemical Biology thanks Fan Jin, Jing Yan and the other, anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Verification of phosphorus-free medium.

a, Schematic of the procedure for planktonic culture. The bacteria were first cultured to log phase in normal M63B1, then we centrifuged and washed the bacteria using phosphorus-free M63B1 for 3 times, and resuspended the bacteria in phosphorus-free M63B1. The resuspended medium was further cultured for another 24 h, then centrifuged and washed using phosphorus-free M63B1 for 3 times before inoculating into M63B1 containing different levels of phosphate. b, Growth curves of planktonic bacteria (prepared according to a) in M63B1 with different levels of phosphate. The bar plot shows OD600 at 24 h. Three biological replicates. Error bars indicate mean values ± SD. Statistical significance was determined by two-sided Student’s t-test.

Source data

Extended Data Fig. 2 The sustained biofilm expansion after phosphate removal was not due to the microfluidics or phosphorus storage.

a-c, To confirm the effectiveness of phosphorus removal, we examined the existence of potential phosphorus sources in the microfluidic chamber. First, we collected the output wastes from the microfluidic chip before and after phosphorus removal, and sent for ion chromatography test (a). Before phosphorus removal, the signal of phosphate could be detected (indicated by the standard sample, phosphoric acid, arrow). After phosphorus removal, no signal of phosphate could be detected. Second, bovine serum albumin (BSA) was used to coat the microfluidic chamber before bacterial loading (Methods). Biofilm expansion rates before and after phosphorus removal were not affected by BSA coating (n = 3 for -BSA group, n = 6 for +BSA group). These results ruled out the possibility of incomplete phosphorus removal from the microfluidic chamber. d-e, Expansion rates of wild type (n = 6 biological replicates), Δppk, Δppx (n = 3 biological replicates) biofilms before and after phosphorus removal. The data points are biological replicates. Statistical significance in relevant panels was determined by two-sided Student’s t-test: ns, not significant, P ≥ 0.05.

Source data

Extended Data Fig. 3 Recycling of phospholipids by the biofilm.

a, Expansion rates of wild type (n = 6 biological replicates), ΔmlaA and ΔyhdP (n = 3 biological replicates) biofilms before phosphorus removal. b, Growth curves of wild type and ΔmlaA in planktonic culture. Six biological replicates. c, Glycerol was used as the solvent for PE stocks. To verify that the glycerol had no effect, we compared biofilm expansion after phosphorus removal with or without 0.5% glycerol (n = 3 for -glycerol group, n = 6 for +glycerol group), and the results showed that supplementation of glycerol had no significant effect on biofilm expansion rate. d-e, Expansion rates of wild type biofilms (n = 6 biological replicates) and knockout strains (ΔpldA, ΔlplT, ΔglpT, ΔugpB, n = 2 biological replicates) related to transport of phospholipid degradation products before and after phosphorus removal. The data points are biological replicates. Statistical significance was determined by two-sided Student’s t-test; ns, not significant, P ≥ 0.05.

Source data

Extended Data Fig. 4 LC-MS/MS results of the abundance of the main phosphorus-containing metabolites in the biofilm supernatant.

a, With or without phosphoserine removal, n = 2 biological replicates. b, With or without 2-AEP removal, n = 2 biological replicates. c, Fold change of phospholipids in biofilm supernatant induced by three types of phosphorus removal (n = 3 for phosphate removal, n = 2 for phosphoserine or 2-AEP removal), 24 h after removal vs. before removal. The data points are biological replicates.

Source data

Extended Data Fig. 5 Control experiments for DCFH-DA and PI.

a, Snapshots of phase contrast (PH), DCFH-DA fluorescence (YFP) and PI fluorescence (mCherry) with or without the addition of DCFH-DA and PI. The white lines indicate the locations of biofilm edge. Scale bar, 100 μm. b, Effect of DCFH-DA and PI on biofilm expansion rate. n = 4 biological replicates. Error bars indicate mean values ± SD. Statistical significance was determined by two-sided Student’s t-test; ns, not significant, P ≥ 0.05.

Source data

Extended Data Fig. 6 ROS-related genetic or chemical perturbations did not affect ROS accumulation, cell death or biofilm expansion rate in normal medium.

a-c, Average DCFH-DA fluorescence (n = 3), PI fluorescence (n = 3), and biofilm expansion rates (n = 6 for wild type biofilms, n = 3 for mutant strains and +DMSO group) before phosphate removal. All data points were biological replicates. d-f, Average DCFH-DA fluorescence, PI fluorescence, and biofilm expansion rate 24 h after 2-AEP removal. n = 2 biological replicates. g-i, Average DCFH-DA fluorescence, PI fluorescence, and biofilm expansion rate before 2-AEP removal. n = 2 biological replicates. Error bars indicate mean values ± SD. Statistical significance in relevant panels was determined by two-sided Student’s t-test; ns, not significant, P ≥ 0.05.

Source data

Extended Data Fig. 7 Cell death after phosphorus reduction.

Average PI fluorescence after various levels of phosphate reduction (for 24 h). The data points are biological replicates.

Source data

Extended Data Fig. 8 Counting percentage of cell death after phosphorus removal.

Bacteria from biofilm or planktonic culture were stained with the fluorescent death marker PI, imaged by fluorescence microscopy. The images are shown under the same contrast setting; representative of 3 biological replicates. Reference dead bacteria (the image on the right) were obtained by killing the bacteria in 80 °C water bath for 20 min. The percentage of cells with high PI fluorescence was calculated at various time points after phosphorus removal. For each condition and time point, > 300 bacteria were counted. Scale bar, 10 μm.

Extended Data Fig. 9 Growth of planktonic bacteria after phosphorus removal.

a, Bacterial dry weight is proportional to the optical density (OD) of the culture, both in normal and in phosphorus-free media. The data points are biological replicates. b, Growth curves of planktonic bacteria. Phosphate was removed at t = 0. This result was used to calculate the corresponding biomass change in Fig. 5d. c, Area of biofilm over time with and without phosphate removal. Arrow indicates the time of phosphorus removal. This result was used to compare with the biomass change of planktonic culture in Fig. 5d. d, Growth curves of bacteria taken from biofilm under normal medium and physically dispersed into individual cells; phosphate was removed at t = 0; this result was used to calculate the corresponding biomass change in Fig. 5d. The fluctuation was due to limited amount of bacteria extracted from the microfluidic chamber. e, PI fluorescence of bacteria cultured in phosphorus-free medium. The definition of planktonic, biofilm to planktonic and biofilm is the same as b-d. These results are representative of 3 biological replicates.

Source data

Extended Data Fig. 10 Validation of biofilm responses after nutrient removal.

a, Confocal images of E. coli biofilms cultivated in flow cell. To help visualize biomass, we constitutively expressed the fluorescent protein sfGFP (green) in the bacteria. Cell death is indicated by PI fluorescence (red). We first cultured the biofilms in normal medium for ~20 h, then switched to medium without phosphate, glucose, or ammonium, respectively. The snapshots shown here were taken right before and 24 h after nutrient removal, respectively (except for the control group). All the snapshots are displayed using the same contrast settings. b-c, Temporal profiles of total PI fluorescence in the biofilm and average biofilm thickness before and after nutrient removal. d, Snapshots of DCFH-DA fluorescence in the biofilm 24 h after nutrient removal. The images are displayed using the same contrast setting as in Fig. 4a. All the results are representative of 3 biological replicates. Scale bar, 100 μm.

Source data

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Wang, Z., Zeng, L., Hu, S. et al. Community-specific cell death sustains bacterial expansion under phosphorus starvation. Nat Chem Biol 21, 867–875 (2025). https://doi.org/10.1038/s41589-024-01796-x

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