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Multiscale X-ray study of Bacillus subtilis biofilms reveals interlinked structural hierarchy and elemental heterogeneity

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Späker,  Oliver
Wolfgang Wagermaier, Biomaterialien, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Scoppola,  Ernesto       
Wolfgang Wagermaier, Biomaterialien, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Azulay, D. N., Späker, O., Ghrayeb, M., Wilsch-Brauninger, M., Scoppola, E., Burghammer, M., et al. (2022). Multiscale X-ray study of Bacillus subtilis biofilms reveals interlinked structural hierarchy and elemental heterogeneity. Proceedings of the National Academy of Sciences of the United States of America, 119(4): e2118107119. doi:10.1073/pnas.2118107119.


Zitierlink: https://hdl.handle.net/21.11116/0000-0008-EF9B-D
Zusammenfassung
Biofilms are multicellular microbial communities that encase themselves in an extracellular matrix (ECM) of secreted biopolymers and attach to surfaces and interfaces. Bacterial biofilms are detrimental in hospital and industrial settings, but they can be beneficial in agricultural contexts. An essential property of biofilms that grants them with increased survival relative to planktonic cells is phenotypic heterogeneity; the division of the biofilm population into functionally distinct subgroups of cells. Phenotypic heterogeneity in biofilms can be traced to the cellular level, however, the molecular structures and elemental distribution across whole biofilms as well as possible linkages between them remain unexplored. Mapping X-ray diffraction (XRD) across intact biofilms in time and space, we revealed the dominant structural features in Bacillus subtilis biofilms, stemming from matrix components, spores and water. By simultaneously following the X-ray fluorescence (XRF) signal of biofilms and isolated matrix components, we discovered that the ECM preferentially binds calcium ions over other metal ions, specifically, zinc, manganese and iron. These ions, remaining free to flow below macroscopic wrinkles that act as water channels, eventually accumulate and lead to sporulation. The possible link between ECM properties, regulation of metal ion distribution and sporulation across whole intact biofilms unravels the importance of molecular-level heterogeneity in shaping biofilm physiology and development.