[ { "id": "authors:fpyjb-qw793", "collection": "authors", "collection_id": "fpyjb-qw793", "cite_using_url": "https://authors.library.caltech.edu/records/fpyjb-qw793", "type": "article", "title": "Extracellular matrix chemistry tunes bacterial biofilm metabolism and optimizes fitness", "author": [ { "family_name": "Li", "given_name": "Jinyang", "orcid": "0000-0003-3190-4021", "clpid": "Li-Jinyang" }, { "family_name": "Squyres", "given_name": "Georgia R.", "orcid": "0000-0002-8717-2897", "clpid": "Squyres-Georgia-R" }, { "family_name": "Duong", "given_name": "Kathy" }, { "family_name": "Reichhardt", "given_name": "Courtney", "orcid": "0000-0002-1022-5110" }, { "family_name": "Parsek", "given_name": "Matthew R.", "orcid": "0000-0003-2932-7966" }, { "family_name": "Newman", "given_name": "Dianne K.", "orcid": "0000-0003-1647-1918", "clpid": "Newman-D-K" } ], "abstract": "Chemically complex extracellular matrices define cellular microenvironments and shape cell behavior across all domains of life. But how has evolution optimized these materials to ensure the success of multicellular communities? Inspired by the well-established composition\u2013properties\u2013function relationships in engineered materials, we hypothesized that analogous relationships exist in extracellular matrices, where the composition and interactions among various matrix components govern material properties and cellular physiology. Here, we examine\n Pseudomonas aeruginosa\n biofilms\u2014representative of ubiquitous multicellular microbial assemblies in nature and disease. We show that electrostatic interactions between the cationic polysaccharide Pel and extracellular DNA (eDNA) compete with eDNA binding to pyocyanin (PYO), a diffusible redox-active metabolite that supports anaerobic metabolism via extracellular electron transfer (EET). From a materials perspective, biofilm-mimetic hydrogels and natural biofilms revealed that altering Pel's charge via pH adjustment or chemical acetylation, or tuning the Pel:eDNA ratio, directly and predictably modulates PYO retention and EET efficiency. Biologically, a lower Pel:eDNA ratio enhances biofilm metabolism under oxygen limitation, whereas a higher ratio promotes survival under antibiotic stress. Notably, these perturbations (pH, Pel structure, and abundance) can be achieved directly or indirectly through biological activities. Together, these findings highlight how biologically regulated matrix chemistry encodes tunable material properties that, in turn, affect cellular responses that confer biofilm fitness advantages. They further suggest cells might actively fine-tune the surrounding matrix chemistry to maximize survival across diverse environments. More broadly, our work establishes a materials-based framework for a mechanistic understanding of the biological functions of extracellular matrix components in multicellular communities.", "doi": "10.1073/pnas.2528666123", "pmcid": "PMC13055754", "issn": "0027-8424", "publisher": "National Academy of Sciences", "publication": "Proceedings of the National Academy of Sciences", "publication_date": "2026-04-14", "series_number": "15", "volume": "123", "issue": "15", "pages": "e2528666123" }, { "id": "authors:kv0hw-5ag59", "collection": "authors", "collection_id": "kv0hw-5ag59", "cite_using_url": "https://authors.library.caltech.edu/records/kv0hw-5ag59", "type": "article", "title": "Single-cell lysis patterns morphogenesis of eDNA in the matrix of Pseudomonas aeruginosa biofilms", "author": [ { "family_name": "Squyres", "given_name": "Georgia R.", "orcid": "0000-0002-8717-2897", "clpid": "Squyres-Georgia-R" }, { "family_name": "Newman", "given_name": "Dianne K.", "orcid": "0000-0003-1647-1918", "clpid": "Newman-D-K" } ], "abstract": "When bacteria form a biofilm, complex behaviors emerge. Biofilm bacteria differ from their free-living counterparts, exhibiting heterogenous, spatiotemporally patterned behavior. Can we explain these patterns by defining the rules that govern single-cell behavior in biofilms? By understanding these rules, can we explain emergent functions at the biofilm scale? Here we reveal how the architecture of extracellular DNA (eDNA) in the biofilm matrix is controlled by single-cell lysis during\n Pseudomonas aeruginosa\n biofilm development. We extend single-cell imaging methods to capture complete biofilm development over 5+ d, characterizing the stages of biofilm development and visualizing eDNA matrix morphogenesis from start to finish. Mapping the spatiotemporal distribution of single-cell lysis events shows that cell lysis is spatiotemporally patterned, concentrated in a region 5 \u00b5m below the biofilm surface that moves with the biofilm as it grows. Using analytical modeling, we examined the consequences of patterning at the biofilm scale. Cell lysis patterning defines eDNA in the matrix: Patterned lysis is sufficient to explain the final eDNA distribution. Cell lysis and biofilm growth are coupled such that the amount of eDNA in the biofilm scales with its volume; this patterning results in a predominantly uniform eDNA matrix architecture, which could not occur without patterning. Finally, we find that patterning of cell lysis is self-organized by nutrient gradients, with maximal lysis occurring in regions where oxygen is present and carbon is limited. The ability of cells to use self-generated nutrient gradients as positioning cues to establish depth-based patterning is a striking feature of bacterial biofilm development.", "doi": "10.1073/pnas.2514210122", "pmcid": "PMC12541396", "issn": "0027-8424", "publisher": "National Academy of Sciences", "publication": "Proceedings of the National Academy of Sciences", "publication_date": "2025-10-14", "series_number": "41", "volume": "122", "issue": "41", "pages": "e2514210122" }, { "id": "authors:9try3-cyw51", "collection": "authors", "collection_id": "9try3-cyw51", "cite_using_url": "https://authors.library.caltech.edu/records/9try3-cyw51", "type": "article", "title": "Biofilms as more than the sum of their parts: lessons from developmental biology", "author": [ { "family_name": "Squyres", "given_name": "Georgia R", "clpid": "Squyres-Georgia-R" }, { "family_name": "Newman", "given_name": "Dianne", "orcid": "0000-0003-1647-1918", "clpid": "Newman-D-K" } ], "abstract": "
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Although our understanding of both bacterial cell physiology and the complex behaviors exhibited by bacterial biofilms is expanding rapidly, we cannot yet sum the behaviors of individual cells to understand or predict biofilm behavior. This is both because cell physiology in biofilms is different from planktonic growth and because cell behavior in biofilms is spatiotemporally patterned. We use developmental biology as a guide to examine this phenotypic patterning, discussing candidate cues that may encode spatiotemporal information and possible roles for phenotypic patterning in biofilms. We consider other questions that arise from the comparison between biofilm and eukaryotic development, including what defines normal biofilm development and the nature of biofilm cell types and fates. We conclude by discussing what biofilm development can tell us about developmental processes, emphasizing the additional challenges faced by bacteria in biofilm development compared with their eukaryotic counterparts.
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", "doi": "10.1016/j.mib.2024.102537", "issn": "1369-5274", "publisher": "Elsevier", "publication": "Current Opinion in Microbiology", "publication_date": "2024-12", "volume": "82", "pages": "102537" } ]