Could DNA uptake be a side effect of bacterial adhesion and twitching motility?

Bakkali, Mohammed

doi:10.1007/s00203-013-0870-1

Cited by 32 publications

(37 citation statements)

References 128 publications

(170 reference statements)

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“…Indeed, on the basis of a fitness disadvantage observed for a pilA − strain on chitin surfaces, it was previously suggested that the Tfp contributes to chitin colonization (15), although these fitness experiments were performed in a quorumsensing-defective strain of V. cholerae that is not naturally transformable. Interestingly, a secondary role for this Tfp would also support a recent hypothesis: Bakkali suggested that DNA uptake might be a side effect of Tfp-mediated bacterial adhesion and twitching motility (42); however, tDNA transfer through the periplasm and across the inner membrane would still require the presence of ComEA, ComEC, and ComF.…”

Section: Discussionsupporting

confidence: 59%

DNA-uptake machinery of naturally competent Vibrio cholerae

Seitz

Blokesch

2013

Proc. Natl. Acad. Sci. U.S.A.

167

247

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Natural competence for transformation is a mode of horizontal gene transfer that is commonly used by bacteria to take up DNA from their environment. As part of this developmental program, so-called competence genes, which encode the components of a DNA-uptake machinery, are expressed. Several models have been proposed for the DNA-uptake complexes of competent bacteria, and most include a type IV (pseudo)pilus as a core component. However, cell-biology-based approaches to visualizing competence proteins have so far been restricted to Gram-positive bacteria. Here, we report the visualization of a competence-induced pilus in the Gram-negative bacterium Vibrio cholerae. We show that piliated cells mostly contain a single pilus that is not biased toward a polar localization and that this pilus colocalizes with the outer membrane secretin PilQ. PilQ, on the other hand, forms several foci around the cell and occasionally colocalizes with the dynamic cytoplasmic-traffic ATPase PilB, which is required for pilus extension. We also determined the minimum competence regulon of V. cholerae, which includes at least 19 genes. Bacteria with mutations in those genes were characterized with respect to the presence of surface-exposed pili, DNA uptake, and natural transformability. Based on these phenotypes, we propose that DNA uptake in naturally competent V. cholerae cells occurs in at least two steps: a pilus-dependent translocation of the incoming DNA across the outer membrane and a pilus-independent shuttling of the DNA through the periplasm and into the cytoplasm.N atural competence for genetic transformation is one of three modes of horizontal gene transfer (HGT) in prokaryotes and is often tightly regulated (1-3). Large pieces of DNA containing a series of genes can be transferred by natural transformation without the need for direct interaction with other microbes or mobile genetic elements. This process can foster rapid evolution, and HGT is known to be involved in the spread of antibiotic resistance, adaptation to new environmental niches, and the emergence of new pathogens.Many bacterial species are able to enter a state of natural competence, including the human pathogen Vibrio cholerae. In this bacterium, competence is induced upon growth on chitinous surfaces (3, 4), the natural habitat of V. cholerae (5). Although we have gained a reasonably clear understanding of the regulatory network driving competence induction in this organism (for a review, see ref.3), almost nothing is known about its DNAuptake machinery. Indeed, the sophisticated DNA-uptake complexes used by naturally competent bacteria during transformation are still poorly characterized (6), especially in Gram-negative bacteria in which the transforming DNA (tDNA) must cross two membranes and the periplasmic space (including the peptidoglycan layer) to enter the cytoplasm and recombine with the chromosome (the latter step is not required if the tDNA consists of plasmid DNA). Interestingly, the majority of competence-protein localization studies using cellu...

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Section: Discussionsupporting

confidence: 59%

DNA-uptake machinery of naturally competent Vibrio cholerae

Seitz

Blokesch

2013

Proc. Natl. Acad. Sci. U.S.A.

167

247

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“…To understand the contribution of the flagellar, the T3SS, and the T4P systems to the survival and movement of strain BS001, we included, next to the wild type, the respective mutant strains of these systems (denoted BS001 ΔfliF , BS001 ΔsctD , and BS001 ΔpilN [4, 5]) in all experiments. The inclusion of the mutants was justified based on previous indications that pH affects the expression and/or function of the T3SS [15–17] and T4P/twitching motility [18, 19], whereas the flagellum is essential for strain BS001 migration in the mycosphere [4]. The cells were introduced at the “tip” or “middle” sites of the hyphal growth front in the soil compartment (denoted introduction site, see “Materials and methods” section).…”

Section: Resultsmentioning

confidence: 99%

Migration of Paraburkholderia terrae BS001 Along Old Fungal Hyphae in Soil at Various pH Levels

2018

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The movement of bacterial cells along with fungal hyphae in soil (the mycosphere) has been reported in several previous studies. However, how local soil conditions affect bacterial migration direction in the mycosphere has not been extensively studied. Here, we investigated the influence of two soil parameters, pH and soil moisture content, on the migration, and survival, of Paraburkholderia terrae BS001 in the mycosphere of Lyophyllum sp. strain Karsten in microcosms containing a loamy sand soil. The data showed that bacterial movement along the hyphal networks took place in both the “forward” and the “backward” directions. Low soil pH strongly restricted bacterial survival, as well as dispersal in both directions, in the mycosphere. The backward movement was weakly correlated with the amount of fungal tissue formed in the old mycelial network. The initial soil moisture content, set at 12 versus 17% (corresponding to 42 and 60% of the soil water holding capacity), also significantly affected the bacterial dispersal along the fungal hyphae. Overall, the presence of fungal hyphae was found to increase the soil pH (under conditions of acidity), which possibly exerted protective effects on the bacterial cells. Finally, we provide a refined model that describes the bacterial migration patterns with fungal hyphae based on the new findings in this study.Electronic supplementary materialThe online version of this article (10.1007/s00248-017-1137-1) contains supplementary material, which is available to authorized users.

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“…Most transformation events are expected to be neutral or deleterious (the latter especially if using DNA from selectively killed cells [25]), and more immediate and reliable benefits of DNA uptake arise from DNA repair and nucleotide acquisition (57). A more extreme view is that DNA uptake could also be in part an unselected consequence of the adhesion and motility activities of T4P (58), though the coordinated regulation of the T4P genes responsible for DNA uptake and the non-T4P genes responsible for translocation into the cytoplasm argues against this. In this context, competence-induced cytoplasmic proteins coregulated with T4P genes take on special importance-are they modulations of the cellular response to their immediate environment or specific adaptations to promote transformation?…”

Section: The Mechanism and Function Of Natural Competencementioning

confidence: 99%

Natural Competence and the Evolution of DNA Uptake Specificity

2014

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Many bacteria are naturally competent, able to actively transport environmental DNA fragments across their cell envelope and into their cytoplasm. Because incoming DNA fragments can recombine with and replace homologous segments of the chromosome, competence provides cells with a potent mechanism of horizontal gene transfer as well as access to the nutrients in extracellular DNA. This review starts with an introductory overview of competence and continues with a detailed consideration of the DNA uptake specificity of competent proteobacteria in the Pasteurellaceae and Neisseriaceae. Species in these distantly related families exhibit strong preferences for genomic DNA from close relatives, a self-specificity arising from the combined effects of biases in the uptake machinery and genomic overrepresentation of the sequences this machinery prefers. Other competent species tested lack obvious uptake bias or uptake sequences, suggesting that strong convergent evolutionary forces have acted on these two families. Recent results show that uptake sequences have multiple "dialects," with clades within each family preferring distinct sequence variants and having corresponding variants enriched in their genomes. Although the genomic consensus uptake sequences are 12 and 29 to 34 bp, uptake assays have found that only central cores of 3 to 4 bp, conserved across dialects, are crucial for uptake. The other bases, which differ between dialects, make weaker individual contributions but have important cooperative interactions. Together, these results make predictions about the mechanism of DNA uptake across the outer membrane, supporting a model for the evolutionary accumulation and stability of uptake sequences and suggesting that uptake biases may be more widespread than currently thought. N aturally competent bacteria actively pull DNA fragments from their environment into their cells. These fragments provide nucleotides, but high similarity with the chromosome also allows them to change the cell's genotype by homologous recombination, a process called natural transformation ( Fig. 1; reviewed in references 1, 2, 3, 4, and 5). Most competent bacteria that have been tested can take up DNA from any source, but species in two distantly related families of Gram-negative bacteria, the Pasteurellaceae and the Neisseriaceae, show strong preferences for DNAs containing short sequences that are highly overrepresented in their own genomes, leading to preferential uptake of conspecific DNA (6). This self-specificity both raises questions about and provides a tool for investigating the evolution of competence and the mechanism of DNA uptake.We begin with a general overview of competence, emphasizing the evolutionary issues. We then describe the two components that together create self-specificity, sequence biases in the DNA uptake machinery and overrepresentation of uptake sequences in the genomes, highlighting recent work on the mechanism and evolution of uptake biases in the two families and an evolutionary model that accounts for upt...

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Could DNA uptake be a side effect of bacterial adhesion and twitching motility?

Cited by 32 publications

References 128 publications

DNA-uptake machinery of naturally competent Vibrio cholerae

DNA-uptake machinery of naturally competent Vibrio cholerae

Migration of Paraburkholderia terrae BS001 Along Old Fungal Hyphae in Soil at Various pH Levels

Natural Competence and the Evolution of DNA Uptake Specificity

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