Genome-scale fitness profile of <i>Caulobacter crescentus</i> grown in natural freshwater

Hentchel, Kristy L.; Ruiz, Leila M. Reyes; Curtis, Patrick D.; Fiebig, Aretha; Coleman, Maureen L.; Crosson, Sean

doi:10.1038/s41396-018-0295-6

Cited by 38 publications

(27 citation statements)

References 51 publications

(72 reference statements)

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“…crescentus CB15. Construction of the library was reported previously, along with its associated statistics (57). Briefly, the transposon pool was introduced into C.…”

Section: Methodsmentioning

confidence: 99%

A Genome-Wide Analysis of Adhesion in Caulobacter crescentus Identifies New Regulatory and Biosynthetic Components for Holdfast Assembly

Hershey

Fiebig

Crosson

2019

mBio

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Bacteria routinely encounter biotic and abiotic materials in their surrounding environments, and they often enlist specific behavioral programs to colonize these materials. Adhesion is an early step in colonizing a surface. Caulobacter crescentus produces a structure called the holdfast which allows this organism to attach to and colonize surfaces. To understand how the holdfast is produced, we performed a genome-wide search for genes that contribute to adhesion by selecting for mutants that could not attach to cheesecloth. We discovered complex interactions between genes that mediate surface contact and genes that contribute to holdfast development. Our genetic selection identified what likely represents a comprehensive set of genes required to generate a holdfast, laying the groundwork for a detailed characterization of the enzymes that build this specialized adhesin.

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“…crescentus CB15. Construction of the library was reported previously, along with its associated statistics (57). Briefly, the transposon pool was introduced into C.…”

Section: Methodsmentioning

confidence: 99%

A Genome-Wide Analysis of Adhesion in Caulobacter crescentus Identifies New Regulatory and Biosynthetic Components for Holdfast Assembly

Hershey

Fiebig

Crosson

2019

mBio

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“…The barcoded HiMar transposon pool APA_752 developed by Wetmore et al (30) was used to create a barcoded Tn library in C. crescentus CB15. Construction of the library has been reported previously along with its associated statistics (57). Briefly, the transposon pool was introduced into C. crescentus by conjugation.…”

Section: Library Development and Mappingmentioning

confidence: 99%

A genome-wide analysis of adhesion inCaulobacter crescentusidentifies new regulatory and biosynthetic components for holdfast assembly

Hershey

Fiebig

Crosson

2018

Preprint

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Due to their intimate physical interactions with the environment, surface polysaccharides are critical determinants of fitness for bacteria. Caulobacter crescentus produces a specialized structure at one of its cell poles called the holdfast that enables attachment to surfaces. Previous studies have shown that the holdfast is a carbohydrate-based material and identified a number of genes required for holdfast development. However, incomplete information about its chemical structure, biosynthetic genes and regulatory principles has limited progress in understanding the mechanism of holdfast synthesis. We have leveraged the adhesive properties of the holdfast to perform a saturating screen for genes affecting attachment to cheesecloth over a multi-day time course. Using similarities in the temporal profiles of mutants in a transposon library, we defined discrete clusters of genes with related effects on cheesecloth colonization. Holdfast synthesis, flagellar motility, type IV pilus assembly and smooth lipopolysaccharide (SLPS) production represented key classes of adhesion determinants. Examining these clusters in detail allowed us to predict and experimentally define the functions of multiple uncharacterized genes in both the holdfast and SLPS pathways. In addition, we showed that the pilus and flagellum control holdfast synthesis separately by modulating the holdfast inhibitor hfiA. This study defines a set of genes contributing to adhesion that includes newly discovered genes required for holdfast biosynthesis and attachment. Our data provide evidence that the holdfast contains a complex polysaccharide with at least four monosaccharides in the repeating unit and underscore the central role of cell polarity in mediating attachment of C. crescentus to surfaces. Importance: Bacteria routinely encounter biotic and abiotic materials in their surrounding environments, and they often enlist specific behavioral programs to colonize these materials. Adhesion is an early step in colonizing a surface. Caulobacter crescentus produces a structure called the holdfast, which allows this organism to attach to and colonize surfaces. To understand how the holdfast is produced, we performed a genome-wide search for genes that contribute to adhesion by selecting for mutants that could not attach to cheesecloth. We discovered complex interactions between genes that mediate surface contact and genes that contribute to holdfast development. Our genetic selection identified what likely represents a comprehensive set of genes required to generate a holdfast, laying the groundwork for a detailed characterization of the enzymes that build this specialized adhesin.

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“…Typically, successful pathogens need to survive in the environment of their hosts [41]. Caulobacter is often described as an oligotroph since it is found in nutrient-poor environments such as fresh-water lakes and drinking water [4,42]. However, our work shows that Caulobacter can also thrive in nutrient-rich culturing conditions (Fig 2).…”

Section: Plos Onementioning

confidence: 70%

Both clinical and environmental Caulobacter species are virulent in the Galleria mellonella infection model

Moore

Gitai

2020

PLoS ONE

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The Caulobacter genus, including the widely-studied model organism Caulobacter crescentus, has been thought to be non-pathogenic and thus proposed as a bioengineering vector for various environmental remediation and medical purposes. However, Caulobacter species have been implicated as the causative agents of several hospital-acquired infections, raising the question of whether these clinical isolates represent an emerging pathogenic species or whether Caulobacters on whole possess previously-unappreciated virulence capability. Given the proposed environmental and medical applications for C. crescentus, understanding the potential pathogenicity of this bacterium is crucial. Consequently, we sequenced a clinical Caulobacter isolate to determine if it has acquired novel virulence determinants. We found that the clinical isolate represents a new species, Caulobacter mirare that, unlike C. crescentus, grows well in standard clinical culture conditions. C. mirare phylogenetically resembles both C. crescentus and the related C. segnis, which was also thought to be non-pathogenic. The similarity to other Caulobacters and lack of obvious pathogenesis markers suggested that C. mirare is not unique amongst Caulobacters and that consequently other Caulobacters may also have the potential to be virulent. We tested this hypothesis by characterizing the ability of Caulobacters to infect the model animal host Galleria mellonella. In this context, two different lab strains of C. crescentus proved to be as pathogenic as C. mirare, while lab strains of E. coli were non-pathogenic. Further characterization showed that Caulobacter pathogenesis in the Galleria model is mediated by lipopolysaccharide (LPS), and that differences in LPS chemical composition across species could explain their differential toxicity. Taken together, our findings suggest that many Caulobacter species can be virulent in specific contexts and highlight the importance of broadening our methods for identifying and characterizing potential pathogens.

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Genome-scale fitness profile of Caulobacter crescentus grown in natural freshwater

Cited by 38 publications

References 51 publications

A Genome-Wide Analysis of Adhesion in Caulobacter crescentus Identifies New Regulatory and Biosynthetic Components for Holdfast Assembly

A Genome-Wide Analysis of Adhesion in Caulobacter crescentus Identifies New Regulatory and Biosynthetic Components for Holdfast Assembly

A genome-wide analysis of adhesion inCaulobacter crescentusidentifies new regulatory and biosynthetic components for holdfast assembly

Both clinical and environmental Caulobacter species are virulent in the Galleria mellonella infection model

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