The Effect of Environmental Conditions on Biofilm Formation of Burkholderia pseudomallei Clinical Isolates

Ramli, Norlisah; Chua, Eng Guan; Nathan, Sheila; Vadivelu, Jamuna

doi:10.1371/journal.pone.0044104

Cited by 62 publications

(52 citation statements)

References 35 publications

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“…5). The effects of temperature on biofilm formation have been reported previously for B. pseudomallei (41) and numerous other bacteria (40). Under our growth conditions over a range of temperatures from 30°C to 42°C, the level of biofilm formation by B. pseudomallei 1026b increased 2-fold at 37°C over that at 30°C but declined sharply at 40°C (Fig.…”

Section: Ggdef-eal Composite Proteinssupporting

confidence: 79%

Thermoregulation of Biofilm Formation in Burkholderia pseudomallei Is Disrupted by Mutation of a Putative Diguanylate Cyclase

et al. 2017

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Burkholderia pseudomallei, a tier 1 select agent and the etiological agent of melioidosis, transitions from soil and aquatic environments to infect a variety of vertebrate and invertebrate hosts. During the transition from an environmental saprophyte to a mammalian pathogen, B. pseudomallei encounters and responds to rapidly changing environmental conditions. Environmental sensing systems that control cellular levels of cyclic di-GMP promote pathogen survival in diverse environments. Cyclic di-GMP controls biofilm production, virulence factors, and motility in many bacteria. This study is an evaluation of cyclic di-GMP-associated genes that are predicted to metabolize and interact with cyclic di-GMP as identified from the annotated genome of B. pseudomallei 1026b. Mutants containing transposon disruptions in each of these genes were characterized for biofilm formation and motility at two temperatures that reflect conditions that the bacteria encounter in the environment and during the infection of a mammalian host. Mutants with transposon insertions in a known phosphodiesterase (cdpA) and a predicted hydrolase (Bp1026b_I2285) gene exhibited decreased motility regardless of temperature. In contrast, the phenotypes exhibited by mutants with transposon insertion mutations in a predicted diguanylate cyclase gene (Bp1026b_II2523) were strikingly influenced by temperature and were dependent on a conserved GG(D/E)EF motif. The transposon insertion mutant exhibited enhanced biofilm formation at 37°C but impaired biofilm formation at 30°C. These studies illustrate the importance of studying behaviors regulated by cyclic di-GMP under varied environmental conditions in order to better understand cyclic di-GMP signaling in bacterial pathogens.IMPORTANCE This report evaluates predicted cyclic di-GMP binding and metabolic proteins from Burkholderia pseudomallei 1026b, a tier 1 select agent and the etiologic agent of melioidosis. Transposon insertion mutants with disruptions in each of the genes encoding these predicted proteins were characterized in order to identify key components of the B. pseudomallei cyclic di-GMP-signaling network. A predicted hydrolase and a phosphodiesterase that modulate swimming motility were identified, in addition to a diguanylate cyclase that modulates biofilm formation and motility in response to temperature. These studies warrant further evaluation of the contribution of cyclic di-GMP to melioidosis in the context of pathogen acquisition from environmental reservoirs and subsequent colonization, dissemination, and persistence within the host.

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Section: Ggdef-eal Composite Proteinssupporting

confidence: 79%

Thermoregulation of Biofilm Formation in Burkholderia pseudomallei Is Disrupted by Mutation of a Putative Diguanylate Cyclase

et al. 2017

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“…B. thailandensis and B. pseudomallei share conserved physiology, including nearly identical QS systems. In agreement with our results for B. thailandensis, QS-1 has been linked to biofilm formation in static biofilm assays of B. pseudomallei (11,12). While the hypothesis still needs to be tested, we predict that QS-1 control of biofilm formation in B. thailandensis E264 has many elements that are conserved in other B. thailandensis strains and in B. pseudomallei.…”

Section: Resultssupporting

confidence: 90%

“…In various species, QS has been shown to play roles in bacterial motility, surface attachment, aggregate formation, biofilm maturation, and biofilm dispersal (8). Within the species Burkholderia, while the role of QS in biofilm formation has been most extensively studied for Burkholderia cepacia complex members (9,10), it has also been demonstrated in Burkholderia pseudomallei (11,12).…”

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confidence: 99%

Quorum Sensing Influences Burkholderia thailandensis Biofilm Development and Matrix Production

et al. 2016

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Members of the genus Burkholderia are known to be adept at biofilm formation, which presumably assists in the survival of these organisms in the environment and the host. Biofilm formation has been linked to quorum sensing (QS) in several bacterial species. In this study, we characterized Burkholderia thailandensis biofilm development under flow conditions and sought to determine whether QS contributes to this process. B. thailandensis biofilm formation exhibited an unusual pattern: the cells formed small aggregates and then proceeded to produce mature biofilms characterized by "dome" structures filled with biofilm matrix material. We showed that this process was dependent on QS. B. thailandensis has three acyl-homoserine lactone (AHL) QS systems (QS-1, QS-2, and QS-3). An AHL-negative strain produced biofilms consisting of cell aggregates but lacking the matrix-filled dome structures. This phenotype was rescued via exogenous addition of the three AHL signals. Of the three B. thailandensis QS systems, we show that QS-1 is required for proper biofilm development, since a btaR1 mutant, which is defective in QS-1 regulation, forms biofilms without these dome structures. Furthermore, our data show that the wild-type biofilm biomass, as well as the material inside the domes, stains with a fucose-binding lectin. The btaR1 mutant biofilms, however, are negative for fucose staining. This suggests that the QS-1 system regulates the production of a fucose-containing exopolysaccharide in wild-type biofilms. Finally, we present data showing that QS ability during biofilm development produces a biofilm that is resistant to dispersion under stress conditions. IMPORTANCEThe saprophyte Burkholderia thailandensis is a close relative of the pathogenic bacterium Burkholderia pseudomallei, the causative agent of melioidosis, which is contracted from its environmental reservoir. Since most bacteria in the environment reside in biofilms, B. thailandensis is an ideal model organism for investigating questions in Burkholderia physiology. In this study, we characterized B. thailandensis biofilm development and sought to determine if quorum sensing (QS) contributes to this process. Our work shows that B. thailandensis produces biofilms with unusual dome structures under flow conditions. Our findings suggest that these dome structures are filled with a QS-regulated, fucose-containing exopolysaccharide that may be involved in the resilience of B. thailandensis biofilms against changes in the nutritional environment. In the environment, many bacteria reside in biofilms. Biofilm growth helps protect the resident bacteria from environmental stresses, such as desiccation, nutrient limitation, and predation (1). Biofilm formation is a coordinated process among community members and can differ from species to species. One key feature of biofilm communities is that they produce an extracellular matrix that serves to hold the community together. This matrix is usually composed of a mixture of extracellular DNA, exopolysaccharides, proteins...

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“…This study also revealed that the expression of biofilm genes and major regulators of biofilm formation is controlled by temperature fluctuations. Low-temperature growth has previously been determined to affect biofilm formation in multiple bacteria (66)(67)(68)(69), and in V. cholerae, temperature affects biofilm formation though the modulation of c-di-GMP signaling by a set of six diguanylate cyclases in V. cholerae (22). Here, we have demonstrated that low-temperature biofilm gene expression is controlled by transcriptional modulation of known biofilm regulators of aphA, hapR, vpsR, and vpsT ( Fig.…”

Section: Discussionmentioning

confidence: 54%

Response of Vibrio cholerae to Low-Temperature Shifts: CspV Regulation of Type VI Secretion, Biofilm Formation, and Association with Zooplankton

Townsley

Mangus

Mehic

et al. 2016

Appl Environ Microbiol

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The ability to sense and adapt to temperature fluctuation is critical to the aquatic survival, transmission, and infectivity of Vibrio cholerae, the causative agent of the disease cholera. Little information is available on the physiological changes that occur when V. cholerae experiences temperature shifts. The genome-wide transcriptional profile of V. cholerae upon a shift in human body temperature (37°C) to lower temperatures, 15°C and 25°C, which mimic those found in the aquatic environment, was determined. Differentially expressed genes included those involved in the cold shock response, biofilm formation, type VI secretion, and virulence. Analysis of a mutant lacking the cold shock gene cspV, which was upregulated >50-fold upon a low-temperature shift, revealed that it regulates genes involved in biofilm formation and type VI secretion. CspV controls biofilm formation through modulation of the second messenger cyclic diguanylate and regulates type VI-mediated interspecies killing in a temperature-dependent manner. Furthermore, a strain lacking cspV had significant defects for attachment and type VI-mediated killing on the surface of the aquatic crustacean Daphnia magna. Collectively, these studies reveal that cspV is a major regulator of the temperature downshift response and plays an important role in controlling cellular processes crucial to the infectious cycle of V. cholerae. IMPORTANCELittle is known about how human pathogens respond and adapt to ever-changing parameters of natural habitats outside the human host and how environmental adaptation alters dissemination. Vibrio cholerae, the causative agent of the severe diarrheal disease cholera, experiences fluctuations in temperature in its natural aquatic habitats and during the infection process. Furthermore, temperature is a critical environmental signal governing the occurrence of V. cholerae and cholera outbreaks. In this study, we showed that V. cholerae reprograms its transcriptome in response to fluctuations in temperature, which results in changes to biofilm formation and type VI secretion system activation. These processes in turn impact environmental survival and the virulence potential of this pathogen.T he facultative human pathogen Vibrio cholerae is found in aquatic reservoirs, such as estuaries, coastal waters, and freshwater lakes and rivers, where it is exposed to seasonal and interannual fluctuations in temperature (1-3). Studies have demonstrated a positive correlation between the occurrence of V. cholerae and surface water temperature in a variety of aquatic environments (4-10) and between cases of the disease cholera and elevated sea surface temperatures in areas where cholera is endemic (5, 6, 11). These aquatic habitats exhibit a temperature range of about 12°C to 30°C (5, 6), whereas the human host environment is a constant 37°C. Temperature is hypothesized to be a key signal to differentiate between host and environmental reservoirs, facilitating virulence factor expression in the human host and genes associated with e...

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The Effect of Environmental Conditions on Biofilm Formation of Burkholderia pseudomallei Clinical Isolates

Cited by 62 publications

References 35 publications

Thermoregulation of Biofilm Formation in Burkholderia pseudomallei Is Disrupted by Mutation of a Putative Diguanylate Cyclase

Thermoregulation of Biofilm Formation in Burkholderia pseudomallei Is Disrupted by Mutation of a Putative Diguanylate Cyclase

Quorum Sensing Influences Burkholderia thailandensis Biofilm Development and Matrix Production

Response of Vibrio cholerae to Low-Temperature Shifts: CspV Regulation of Type VI Secretion, Biofilm Formation, and Association with Zooplankton

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