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A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm.

ABSTRACT: In natural systems, bacteria form complex, surface-attached communities known as biofilms. This lifestyle presents numerous advantages compared with unattached or planktonic life, such as exchange of nutrients, protection from environmental stresses and increased tolerance to biocides. Despite such benefits, dispersal also plays an important role in escaping deteriorating environments and in successfully colonizing favourable, unoccupied habitat patches. The ?-proteobacterium Caulobacter crescentus produces a motile swarmer cell and a sessile stalked cell at each cell division. We show here that C. crescentus extracellular DNA (eDNA) inhibits the ability of its motile cell type to settle in a biofilm. eDNA binds to the polar holdfast, an adhesive structure required for permanent surface attachment and biofilm formation, thereby inhibiting cell attachment. Because stalked cells associate tightly with the biofilm through their holdfast, we hypothesize that this novel mechanism acts on swarmer cells born in a biofilm, where eDNA can accumulate to a sufficient concentration to inhibit their ability to settle. By targeting a specific cell type in a biofilm, this mechanism modulates biofilm development and promotes dispersal without causing a potentially undesirable dissolution of the existing biofilm.

SUBMITTER: Berne C

PROVIDER: S-EPMC2962764 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm.

Berne Cécile C Kysela David T DT Brun Yves V YV

Molecular microbiology 20100628 4

In natural systems, bacteria form complex, surface-attached communities known as biofilms. This lifestyle presents numerous advantages compared with unattached or planktonic life, such as exchange of nutrients, protection from environmental stresses and increased tolerance to biocides. Despite such benefits, dispersal also plays an important role in escaping deteriorating environments and in successfully colonizing favourable, unoccupied habitat patches. The α-proteobacterium Caulobacter crescen ...[more]

PMID: 20598083

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Project description:Campylobacter jejuni is a microaerophilic bacterium and is believed to persist in a biofilm to antagonize environmental stress. This study investigated the influence of environmental conditions on the formation of C. jejuni biofilm. We report an extracellular DNA (eDNA)-mediated mechanism of biofilm formation in response to aerobic and starvation stress. The eDNA was determined to represent a major form of constitutional material of C. jejuni biofilms and to be closely associated with bacterial lysis. Deletion mutation of the stress response genes spoT and recA enhanced the aerobic influence by stimulating lysis and increasing eDNA release. Flagella were also involved in biofilm formation but mainly contributed to attachment rather than induction of lysis. The addition of genomic DNA from either Campylobacter or Salmonella resulted in a concentration-dependent stimulation effect on biofilm formation, but the effect was not due to forming a precoating DNA layer. Enzymatic degradation of DNA by DNase I disrupted C. jejuni biofilm. In a dual-species biofilm, eDNA allocated Campylobacter and Salmonella at distinct spatial locations that protect Campylobacter from oxygen stress. Our findings demonstrated an essential role and multiple functions of eDNA in biofilm formation of C. jejuni, including facilitating initial attachment, establishing and maintaining biofilm, and allocating bacterial cells.IMPORTANCECampylobacter jejuni is a major cause of foodborne illness worldwide. In the natural environment, the growth of C. jejuni is greatly inhibited by various forms of environmental stress, such as aerobic stress and starvation stress. Biofilm formation can facilitate the distribution of C. jejuni by enabling the survival of this fragile microorganism under unfavorable conditions. However, the mechanism of C. jejuni biofilm formation in response to environmental stress has been investigated only partially. The significance of our research is in identifying extracellular DNA released by bacterial lysis as a major form of constitution material that mediates the formation of C. jejuni biofilm in response to environmental stress, which enhances our understanding of the formation mechanism of C. jejuni biofilm. This knowledge can aid the development of intervention strategies to limit the distribution of C. jejuni.

Dataset Information

A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm.

Publications

A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm.

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