Following the terrestrial tracks of <i>Caulobacter</i> - redefining the ecology of a reputed aquatic oligotroph

Wilhelm, Roland C.

doi:10.1038/s41396-018-0257-z

Cited by 65 publications

(41 citation statements)

References 96 publications

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“…In addition to the four MCP-encoding genes present in the two chemotaxis operons, there are also 14 independent genes coding for putative MCPs (Table 1), suggesting that C. crescentus may sense a large array of specific attractants. The presence of a large number of MCPs in its genome is consistent with Caulobacter being a bacterium abundantly found in oligotrophic freshwater and nutrient-rich soil environments (51, 52). There are also several copies of key chemotaxis genes scattered in the genome, such as six copies of cheY , two of cheW , and one extra cheR (Table 1).…”

Section: Resultssupporting

confidence: 58%

The two chemotaxis inCaulobacter crescentusoperons play different roles in chemotaxis and biofilm regulation

Berne

Brun

2019

Preprint

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The two chemotaxis in Caulobacter crescentus operons play different roles in 2 chemotaxis and biofilm regulation. 3 4 5 RUNNING TITLE 6 Chemotaxis and biofilm regulation in Caulobacter crescentus. 7 8 9 AUTHORS 10 ABSTRACT 22The holdfast polysaccharide adhesin is crucial for irreversible cell adhesion and 23 biofilm formation in Caulobacter crescentus. Holdfast production is tightly controlled via 24 developmental regulators, and environmental and physical signals. Here we identified a 25 novel mechanism of holdfast production regulation that involves chemotaxis proteins. 26We characterized the two identified chemotaxis operons of C. crescentus and showed 27 that only the previously characterized, major operon is involved in chemotactic response 28 towards different carbon sources. However, both chemotaxis operons encoded in the C. 29 crescentus genome play a role in biofilm formation and holdfast production, by 30 regulating the expression of hfiA, the gene encoding the holdfast inhibitor HfiA. We 31show that CheA and CheB proteins act in an antagonistic manner: while the two CheA 32 proteins negatively regulate hfiA expression, the CheB proteins are positive regulators, 33 thus providing a modulation of holdfast synthesis and surface attachment. 34 35 36 IMPORTANCE 37Chemosensory pathways are major signal transduction mechanisms in bacteria. 38These systems are involved in chemotaxis and other cell responses to environment 39 conditions, such as production of adhesins that enable irreversible adhesion to a 40 surface and surface colonization. The C. crescentus genome encodes two complete 41 chemotaxis operons. Here we characterized the second, novel chemotaxis-like operon. 42While only the major chemotaxis operon is involved in chemotaxis, both chemotaxis 43 systems modulate C. crescentus adhesion by controlling expression of the holdfast synthesis inhibitor, HfiA. Thus, we identified a new level in holdfast regulation, providing 45 new insights into the control of adhesin production that leads to the formation of 46 biofilms. 47The central chemotaxis system is composed of a chemoreceptor, or methyl-68 accepting chemotaxis protein (MCP), and CheW, CheA, and CheY proteins (13)(14)(15)(16). 69Complexes of these proteins form hexagonally packed arrays localized at the cell pole. 70MCPs are transmembrane proteins, while CheW, CheA, and CheY are located in the 71 cytoplasm (17, 18). Chemotactic signals are sensed by the MCPs and transduced to the 72 sensory histidine kinase CheA, which is linked to the MCP via the scaffolding protein 73 CheW (Fig. 1A). CheA autophosporylates upon receiving the signal and rapidly 74 transfers its phosphate to the CheY response regulator, which modulates flagellum 75 rotation. CheA can also transmit its phosphate to the methylesterase CheB, at a slower 76 rate than the transfer to CheY. CheB~P is activated and removes a methyl group from 77 the MCP, reducing the activity of the signal transduction cascade to control the MCP 78 adaptation process that allows the signal to be reset to a...

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Section: Resultssupporting

confidence: 58%

The two chemotaxis inCaulobacter crescentusoperons play different roles in chemotaxis and biofilm regulation

Berne

Brun

2019

Preprint

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“…The presence of a large number of MCPs in its genome is consistent with Caulobacter spp. being bacteria abundantly found in environments as diverse as oligotrophic freshwaters and nutrient-rich soils and being exposed to a wide array of attractants and repellent molecules (59,60). No cheC, cheV, or cheZ homologs were detected in the C. crescentus genome ( Table 1).…”

Section: Resultsmentioning

confidence: 99%

The Two Chemotaxis Clusters in Caulobacter crescentus Play Different Roles in Chemotaxis and Biofilm Regulation

Berne

Brun

2019

J Bacteriol

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The holdfast polysaccharide adhesin is crucial for irreversible cell adhesion and biofilm formation in Caulobacter crescentus. Holdfast production is tightly controlled via developmental regulators, as well as via environmental and physical signals. Here, we identify a novel mode of regulation of holdfast synthesis that involves chemotaxis proteins. We characterized the two identified chemotaxis clusters of C. crescentus and showed that only the previously characterized major cluster is involved in the chemotactic response toward different carbon sources. However, both chemotaxis clusters encoded in the C. crescentus genome play a role in biofilm formation and holdfast production by regulating the expression of hfiA, the gene encoding the holdfast inhibitor HfiA. We show that CheA and CheB proteins act in an antagonistic manner, as follows: while the two CheA proteins negatively regulate hfiA expression, the CheB proteins are positive regulators, thus providing a modulation of holdfast synthesis and surface attachment. IMPORTANCE Chemosensory systems constitute major signal transduction pathways in bacteria. These systems are involved in chemotaxis and other cell responses to environment conditions, such as the production of adhesins to enable irreversible adhesion to a surface and surface colonization. The C. crescentus genome encodes two complete chemotaxis clusters. Here, we characterized the second novel chemotaxis-like cluster. While only the major chemotaxis cluster is involved in chemotaxis, both chemotaxis systems modulate C. crescentus adhesion by controlling expression of the holdfast synthesis inhibitor HfiA. Here, we identify a new level in holdfast regulation, providing new insights into the control of adhesin production that leads to the formation of biofilms in response to the environment.

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“…Briefly, C. crescentus is among a group of dimorphic prosthecate (i.e., stalked) bacteria that attach to surfaces, often forming epibiotic interactions with algae and plant material [11]. More broadly, members of the genus Caulobacter are common in soil ecosystems, where they likely play an important role in plant matter decomposition [12]. In aquatic systems, Caulobacter interactions with substrates contribute to biopolymer mineralization, and have been proposed to enhance productivity of aquatic ecosystems [11,13].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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Bacterial genomes evolve in complex ecosystems and are best understood in this natural context, but replicating such conditions in the lab is challenging. We used transposon sequencing to define the fitness consequences of gene disruption in the bacterium Caulobacter crescentus grown in natural freshwater, compared with axenic growth in common laboratory media. Gene disruptions in amino-acid and nucleotide sugar biosynthesis pathways and in metabolic substrate transport machinery impaired fitness in both lake water and defined minimal medium relative to complex peptone broth. Fitness in lake water was enhanced by insertions in genes required for flagellum biosynthesis and reduced by insertions in genes involved in biosynthesis of the holdfast surface adhesin. We further uncovered numerous hypothetical and uncharacterized genes for which disruption impaired fitness in lake water, defined minimal medium, or both. At the genome scale, the fitness profile of mutants cultivated in lake water was more similar to that in complex peptone broth than in defined minimal medium. Microfiltration of lake water did not significantly affect the terminal cell density or the fitness profile of the transposon mutant pool, suggesting that Caulobacter does not strongly interact with other microbes in this ecosystem on the measured timescale. Fitness of select mutants with defects in cell surface biosynthesis and environmental sensing were significantly more variable across days in lake water than in defined medium, presumably owing to day-to-day heterogeneity in the lake environment. This study reveals genetic interactions between Caulobacter and a natural freshwater environment, and provides a new avenue to study gene function in complex ecosystems.

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Following the terrestrial tracks of Caulobacter - redefining the ecology of a reputed aquatic oligotroph

Cited by 65 publications

References 96 publications

The two chemotaxis inCaulobacter crescentusoperons play different roles in chemotaxis and biofilm regulation

The two chemotaxis inCaulobacter crescentusoperons play different roles in chemotaxis and biofilm regulation

The Two Chemotaxis Clusters in Caulobacter crescentus Play Different Roles in Chemotaxis and Biofilm Regulation

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

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