Cellular arrangement impacts metabolic activity and antibiotic tolerance in Pseudomonas aeruginosa biofilms.

Cellular arrangement impacts metabolic activity and antibiotic tolerance in Pseudomonas aeruginosa biofilms.
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DOI:
10.1371/journal.pbio.3002205
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发表时间:
2024-02
期刊:
影响因子:
9.8
通讯作者:
Dietrich, Lars E. P.
Dietrich, Lars E. P.
中科院分区:
生物学1区
文献类型:
--
作者:
Dayton, Hannah;Kiss, Julie;Wei, Mian;Chauhan, Shradha;LaMarre, Emily;Cornell, William Cole;Morgan, Chase J.;Janakiraman, Anuradha;Min, Wei;Tomer, Raju;Price-Whelan, Alexa;Nirody, Jasmine A.;Dietrich, Lars E. P.

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Cells must access resources to survive, and the anatomy of multicellular structures influences this access. In diverse multicellular eukaryotes, resources are provided by internal conduits that allow substances to travel more readily through tissue than they would via diffusion. Microbes growing in multicellular structures, called biofilms, are also affected by differential access to resources and we hypothesized that this is influenced by the physical arrangement of the cells. In this study, we examined the microanatomy of biofilms formed by the pathogenic bacterium Pseudomonas aeruginosa and discovered that clonal cells form striations that are packed lengthwise across most of a mature biofilm’s depth. We identified mutants, including those defective in pilus function and in O-antigen attachment, that show alterations to this lengthwise packing phenotype. Consistent with the notion that cellular arrangement affects access to resources within the biofilm, we found that while the wild type shows even distribution of tested substrates across depth, the mutants show accumulation of substrates at the biofilm boundaries. Furthermore, we found that altered cellular arrangement within biofilms affects the localization of metabolic activity, the survival of resident cells, and the susceptibility of subpopulations to antibiotic treatment. Our observations provide insight into cellular features that determine biofilm microanatomy, with consequences for physiological differentiation and drug sensitivity. Cells must access resources to survive, and the anatomy of multicellular structures influences this access. This study shows that bacteria in biofilms divide along oxygen gradients; their end-to-end patterning affects how molecules move through the biofilm, and therefore the physiology and drug susceptibility of biofilm subzones.
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