Multifaceted roles of extracellular DNA in bacterial physiology

Vorkapić, Dina; Preßler, Katharina; Schild, Stefan

doi:10.1007/s00294-015-0514-x

Cited by 106 publications

(84 citation statements)

References 121 publications

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“…In addition to the role of secreted DNA in the transfer of genetic information, other roles, such as acting as a nutrient source or as an important structural component of biofilms have been suggested (For review see: Vorkapic et al 2016). At the onset of biofilm formation, the initially planktonic bacteria attach reversibly to the surface and start to produce an extracellular matrix of polymeric substances, which results in their irreversible attachment to the surface (Dunne 2002).…”

Section: Secreted Dna Affects Biofilm Formationmentioning

confidence: 99%

“…These polymeric substances can consist of exopolysaccharides, secreted proteins, membrane vesicles or extracellular DNA. For many bacteria, including N. gonorrhoeae , it was demonstrated that extracellular DNA is an important component of the biofilm (Steichen et al 2011; Zweig et al 2014; Vorkapic et al 2016). Growth of N. gonorrhoeae MS11 biofilms in a medium containing Exonuclease I, which specifically degrades ssDNA, delayed biofilm formation in its initial phases (Zweig et al 2014).…”

Section: Secreted Dna Affects Biofilm Formationmentioning

confidence: 99%

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Secretion of Chromosomal DNA by the Neisseria gonorrhoeae Type IV Secretion System

Callaghan

Heilers

Does

et al. 2017

Current Topics in Microbiology and Immunology

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Approximately 80% of Neisseria gonorrhoeae and 17.5% of Neisseria meningitidis clinical isolates carry a ~59 kb genomic island known as the gonococcal genetic island (GGI). About half of the GGI consists of genes encoding a type IV secretion system (T4SS), and most of these genes are clustered in a ~28 kb region at one end of the GGI. Two additional genes (parA and parB) are found at the other end of the island. The remainder of the GGI consists mostly of hypothetical proteins, with several being identified as DNA binding or processing proteins. The T4SS genes show similarity to those of the F-plasmid family of conjugation systems, with similarity in gene order and a low but significant level of sequence identity for the encoded proteins. However, several GGI-encoded proteins are unique from the F-plasmid system, such as AtlA, Yag, and TraA. Interestingly, the gonococcal T4SS does not act as a conjugation system. Instead, this T4SS secretes ssDNA into the extracellular milieu, where it can serve to transform highly competent Neisseria species, thereby increasing the transfer of genetic information. Although many of the T4SS proteins are expressed at low levels, this system has been implicated in several cellular processes. The secreted ssDNA is involved in the initial stages of biofilm formation, and the presence of the T4SS enables TonB-independent intracellular survival of N. gonorrhoeae strains during infection of cervical cells. Other GGI-like T4SS have been identified in several other α-, β- and γ-Proteobacteria, but the function of these GGI-like T4SSs is unknown. Remarkably, the presence of the GGI is related to resistance to several antibiotics. Here we describe our current knowledge about the GGI and its unique ssDNA-secreting T4SS.

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Section: Secreted Dna Affects Biofilm Formationmentioning

confidence: 99%

Section: Secreted Dna Affects Biofilm Formationmentioning

confidence: 99%

Secretion of Chromosomal DNA by the Neisseria gonorrhoeae Type IV Secretion System

Callaghan

Heilers

Does

et al. 2017

Current Topics in Microbiology and Immunology

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“…More specifically, why does evolution favor and preserve a trait that is energy intensive and at the expense of the life of some cells within a pneumococcus population (by allolysis) but does not show immediate advantages? Indeed, despite its contribution to horizontal gene transfer (Vorkapic et al 2015), genetic transformation in itself has been shown to be dispensable for infection, as proven by the lack of virulence loss after deletion of genes essential for DNA uptake and recombination (Zhu et al , 2015. Excitingly, the first evidence which directly supports the X-state-for-fitness model was shown by our recently published study that distinguishes between competence-dependent 'late' genes that contribute to pneumococcal fitness versus those that are competence-independent (Zhu et al 2015).…”

Section: Introductionmentioning

confidence: 98%

Disentangling competence for genetic transformation and virulence in Streptococcus pneumoniae

2015

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Horizontal gene transfer mediated by the competence regulon is a major driver of genome plasticity in Streptococcus pneumoniae. When pneumococcal cells enter the competent state, about 6% of the genes in the genome are up-regulated. Among these, some genes are essential for genetic transformation while others are dispensable for the process. Exhaustive deletion analyses show that some up-regulated genes dispensable for genetic transformation contribute to pneumococcal-mediated pneumonia and bacteremia infections. Interestingly, virulence functions of such genes are either dependent or independent of the competent state. Among the competent-state-dependent genes are those mediating allolysis, a process where small fraction of non-competent cells within the pneumococcal population are lysed by their competent counterparts, releasing DNA presumably for transformation. Inadvertently, the pore-forming toxin pneumolysin is also released during allolysis, contributing to virulence. In this review, we discuss recent advances in our understanding of pneumococcal virulence processes mediated by the competence regulon. We proposed that coupling of competence induction and bacterial fitness drives the natural selection to favor an intact competence regulon, which in turn, provides the long-term benefits of genetic plasticity.

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“…The DNA molecule has been previously described as a nutrient source, for recombination into the chromosome, for repair of the cell’s own DNA or as a building element in bacterial biofilms (Vorkapic et al, 2016). Nevertheless, theses physiological roles are attributed to DNA molecules found outside of the cell, also known as extracellular DNA (eDNA).…”

Section: Introductionmentioning

confidence: 99%

A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms

et al. 2016

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The DNA molecule is associated with the role of encoding information required to produce RNA which is translated into proteins needed by the cell. This encoding involves information transmission to offspring or to other organisms by horizontal transfer. However, despite the abundance of this molecule in both the cell and the environment, its physiological role seems to be restricted mainly to that of a coding and inheritance molecule. In this paper, we report a new physiological role for the DNA molecule as involved in protection against desiccation, in addition to its well-established main information transfer and other recently reported functions such as bio-film formation in eDNA form. Desiccation-tolerant microorganisms such as Microbacterium sp. 3J1 significantly upregulate genes involved in DNA synthesis to produce DNA as part of their defensive mechanisms to protect protein structures and functions from drying according to RNA-seq analysis. We have observed the intracellular overproduction of DNA in two desiccation-tolerant microorganisms, Microbacterium sp. 3J1 and Arthrobacter siccitolerans 4J27, in response to desiccation signals. In addition, this conclusion can be made from our observations that synthetic DNA protects two proteins from drying and when part of a xeroprotectant preparation, DNA from various organisms including desiccation-sensitive species, does the same. Removal of DNA by nuclease treatment results in absence of this additive protective effect. We validated this role in biochemical and biophysical assays in proteins and occurs in trans even with short, single chains of synthetically produced DNA.

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Multifaceted roles of extracellular DNA in bacterial physiology

Cited by 106 publications

References 121 publications

Secretion of Chromosomal DNA by the Neisseria gonorrhoeae Type IV Secretion System

Secretion of Chromosomal DNA by the Neisseria gonorrhoeae Type IV Secretion System

Disentangling competence for genetic transformation and virulence in Streptococcus pneumoniae

A New Physiological Role for the DNA Molecule as a Protector against Drying Stress in Desiccation-Tolerant Microorganisms

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