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A cold-responsive fimACD chaperone-usher operon tunes motility and biofilm formation in Pseudomonas fragi D12.

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Title: A cold-responsive fimACD chaperone-usher operon tunes motility and biofilm formation in Pseudomonas fragi D12.
Authors: Li, Shaoyu1,2, Zhang, Xia1,2, Li, Murong1,2, Zhou, Meng1,2, Xing, Zhihao1,2, Zhu, Wenbo3, Liu, Yehui1,2, Li, Qiyun1 liqiyun@jlau.edu.cn, Zang, Xueli4 2296415080@qq.com, Zhang, Sitong1,2 18943132269@163.com
Source: Applied & Environmental Microbiology. May2026, Vol. 92 Issue 5, p1-18. 18p.
Subjects: Cold adaptation, Operons, Biofilms, Cell motility, Bacterial adhesion, Pseudomonas, RNA sequencing
Abstract: Low temperature alters bacterial growth and surface-linked behaviors; however, the genetic role of the associated pilus systems in cold adaptation remains unclear. Here, we used the psychrotolerant tundra isolate Pseudomonas fragi D12 as a model to investigate the transcriptional responses and functional divergence of three fimbrial genes, fimA, fimC, and fimD, through a combination of transcriptome analysis and gene knockout/overexpression assays. RNA-seq analysis revealed that extreme cold stress (4°C) triggered a robust induction of the fim cluster and an adjacent regulatory module comprising an Arc-family DNA-binding protein and an EAL-domain phosphodiesterase. qRT-PCR confirmed the RNA-seq trends. Functional assays demonstrated distinct ecological roles; deletion of fimA increased swimming but reduced swarming, whereas overexpression of fimA led to an increase in swarming. fimC overexpression enhanced swimming, whereas fimC deletion decreased swarming. fimD deletion increased swimming and reduced swarming, while fimD overexpression suppressed swarming. Temperature-gradient experiments further showed that across the three temperatures examined (4°C, 15°C, and 30°C), motility and biofilm formation were the highest at 15°C. Transmission electron microscopy associated these behavioral changes with altered fimbrial density and organization, and growth-curve analysis indicated no major defects in planktonic proliferation. In combination, the data point to a fimbri al apparatus that is transcriptionally responsive to cold and may mechanically modulate the coupling of a single polar flagellum to liquid and solid interfaces, while the genomic context of fimACD remains compatible with local modulation of cyclic di-GMP signaling that has yet to be examined directly. [ABSTRACT FROM AUTHOR]
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Database: Engineering Source
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Abstract:Low temperature alters bacterial growth and surface-linked behaviors; however, the genetic role of the associated pilus systems in cold adaptation remains unclear. Here, we used the psychrotolerant tundra isolate Pseudomonas fragi D12 as a model to investigate the transcriptional responses and functional divergence of three fimbrial genes, fimA, fimC, and fimD, through a combination of transcriptome analysis and gene knockout/overexpression assays. RNA-seq analysis revealed that extreme cold stress (4°C) triggered a robust induction of the fim cluster and an adjacent regulatory module comprising an Arc-family DNA-binding protein and an EAL-domain phosphodiesterase. qRT-PCR confirmed the RNA-seq trends. Functional assays demonstrated distinct ecological roles; deletion of fimA increased swimming but reduced swarming, whereas overexpression of fimA led to an increase in swarming. fimC overexpression enhanced swimming, whereas fimC deletion decreased swarming. fimD deletion increased swimming and reduced swarming, while fimD overexpression suppressed swarming. Temperature-gradient experiments further showed that across the three temperatures examined (4°C, 15°C, and 30°C), motility and biofilm formation were the highest at 15°C. Transmission electron microscopy associated these behavioral changes with altered fimbrial density and organization, and growth-curve analysis indicated no major defects in planktonic proliferation. In combination, the data point to a fimbri al apparatus that is transcriptionally responsive to cold and may mechanically modulate the coupling of a single polar flagellum to liquid and solid interfaces, while the genomic context of fimACD remains compatible with local modulation of cyclic di-GMP signaling that has yet to be examined directly. [ABSTRACT FROM AUTHOR]
ISSN:00992240
DOI:10.1128/aem.02472-25