Adaptive responses to antimicrobial agents in biofilms

Szomolay, Barbara; Klapper, Isaac; Dockery, Jack D.; Stewart, Philip S.

doi:10.1111/j.1462-2920.2005.00797.x

Cited by 120 publications

(109 citation statements)

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“…Our results show that exponential-and stationary-phase planktonic cells of Z. mobilis were equally susceptible to benzaldehyde, indicating that benzaldehyde resistance was not growth rate dependent for planktonic cells. In general, increased resistance in biofilms may be a result of altered gene expression which leads to physiological and/or structural changes during biofilm formation (17,31,33,38). It is possible that the benzaldehyde resistance of Z. mobilis biofilms is conferred by, for example, benzaldehyde excretion or altered membrane composition to counteract any benzaldehyde effect on membrane fluidity.…”

Section: Discussionmentioning

confidence: 99%

“…Bacteria in biofilms can differ profoundly in terms of phenotypic characteristics (31,33) or adaptive responses to stress (17,38) from their planktonic counterparts, which can provide survival advantages and protection in a range of environmental conditions (16,23). Biofilms are also commonly found on medical implants and are responsible for many persistent infections due to their increased resistance to antimicrobial agents (13).…”

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confidence: 99%

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Enhanced Benzaldehyde Tolerance in Zymomonas mobilis Biofilms and the Potential of Biofilm Applications in Fine-Chemical Production

Li¹,

Webb

Kjelleberg

et al. 2006

Appl Environ Microbiol

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Biotransformation plays an increasingly important role in the industrial production of fine chemicals due to its high product specificity and low energy requirement. One challenge in biotransformation is the toxicity of substrates and/or products to biocatalytic microorganisms and enzymes. Biofilms are known for their enhanced tolerance of hostile environments compared to planktonic free-living cells. Zymomonas mobilis was used in this study as a model organism to examine the potential of surface-associated biofilms for biotransformation of chemicals into value-added products. Z. mobilis formed a biofilm with a complex three-dimensional architecture comprised of microcolonies with an average thickness of 20 m, interspersed with water channels. Microscopic analysis and metabolic activity studies revealed that Z. mobilis biofilm cells were more tolerant to the toxic substrate benzaldehyde than planktonic cells were. When exposed to 50 mM benzaldehyde for 1 h, biofilm cells exhibited an average of 45% residual metabolic activity, while planktonic cells were completely inactivated. Three hours of exposure to 30 mM benzaldehyde resulted in sixfold-higher residual metabolic activity in biofilm cells than in planktonic cells. Cells inactivated by benzaldehyde were evenly distributed throughout the biofilm, indicating that the resistance mechanism was different from mass transfer limitation. We also found that enhanced tolerance to benzaldehyde was not due to the conversion of benzaldehyde into less toxic compounds. In the presence of glucose, Z. mobilis biofilms in continuous cultures transformed 10 mM benzaldehyde into benzyl alcohol at a steady rate of 8.11 g (g dry weight)؊1 day ؊1 with a 90% molar yield over a 45-h production period.Microbes in nature are commonly in surface-associated, matrix-enclosed structures referred to as biofilms (7,28). Bacteria in biofilms can differ profoundly in terms of phenotypic characteristics (31, 33) or adaptive responses to stress (17, 38) from their planktonic counterparts, which can provide survival advantages and protection in a range of environmental conditions (16,23). Biofilms are also commonly found on medical implants and are responsible for many persistent infections due to their increased resistance to antimicrobial agents (13).While deleterious in clinical settings, biofilms are of great interest in biotechnology. For example, biofilms have been used as biocatalysts in bioremediation and wastewater treatment processes (21,23,27) and in fermentative vinegar (9) and ethanol (20) production from agricultural materials, as well as in biosynthesis of polymers (42). To our knowledge, the use of biofilms for transformation of fine chemicals into value-added products has not been reported previously.Biotransformation using viable cells capable of cofactor regeneration is an important approach to fine-chemical production (30, 34). A common obstacle in biocatalytic fine-chemical production is the potential toxic effects of substrates and/or products on cells during the process. S...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Enhanced Benzaldehyde Tolerance in Zymomonas mobilis Biofilms and the Potential of Biofilm Applications in Fine-Chemical Production

Li¹,

Webb

Kjelleberg

et al. 2006

Appl Environ Microbiol

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“…Bacteria with biofilms may have an increased resistance to antimicrobials, ambient pressure and the host immune system (Arciola et al, 2001;Costerton et al, 2003;Szomolay et al, 2005). In order to understand the relationship between biofilms and antimicrobial resistance in S. Pullorum, we assayed the ability of the isolates to form biofilms.…”

Section: Discussionmentioning

confidence: 99%

Antimicrobial resistance, presence of integrons and biofilm formation ofSalmonellaPullorum isolates from eastern China (1962–2010)

Gong

Zhu

et al. 2013

Avian Pathology

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Three hundred and thirty-seven isolates of Salmonella Pullorum from eastern China between 1962 and 2010 were characterized for antimicrobial susceptibility (disk diffusion method), the presence of integrons (polymerase chain reaction followed by sequencing) and the ability to form biofilms (semi-quantitative adherence assay). Two hundred and fifty-eight isolates (76.6%) exhibited multiple drug resistance (MDR; resistant to at least three different classes of antimicrobials), and the level of drug resistance is increasing with time. There were three isolates (9.4%) exhibiting MDR from 1962 to 1968. MDR rates began to increase for isolates between 1970 to 1979 and 1980 to 1987 (64.6 to 78.7%). The MDR rates reached 96.6% for isolates between 1990 and 2010. Polymerase chain reaction screening for integrons showed that 75 isolates (22.3%) were positive for class 1 integrons while none were positive for class 2 integrons. All of the class 1 integron-positive isolates exhibited MDR and were more frequently resistant than the negative isolates. Two hundred and twenty isolates (65.3%) had the ability to form biofilms, and bacterial resistance levels to cefamandole, trimethoprim and trimethoprim/sulfamethoxazole were significantly higher for biofilm-positive groups than the biofilm-negative groups. Our data show that multidrug resistance is common among S. Pullorum isolated from eastern China, being more frequent after 1990 than before 1990, and the presence of class 1 integrons is associated with multidrug resistance.

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“…O'Toole and Kolter reported that protein synthesis was required for initiation of biofilm formation in Pseudomonas fluorescens WCS365 (36). Treatment of chloramphenicol at the onset of biofilm formation might affect the protein synthesis or the activity of some regulatory proteins, which in turn would affect its biofilm development and produce induction cues for larval settlement, while after 10 h of development, those proteins that were required for presenting larval settlement induction might have already been synthesized (50), which in turn would maintain the biofilm's ability to induce larval settlement. The surface protein profiles of YP-grown P. spongiae and Pgrown P. spongiae before attachment and after 10 h of attachment were then further investigated.…”

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confidence: 99%

Effect of Biofilm Formation by Pseudoalteromonas spongiae on Induction of Larval Settlement of the Polychaete Hydroides elegans

Huang

Dobretsov

Xiong

et al. 2007

Appl Environ Microbiol

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The effects of culture conditions and chloramphenicol treatment on the induction of the marine bacterium Pseudoalteromonas spongiae to larval settlement of Hydroides elegans were investigated. The results showed that P. spongiae cells grown in the medium containing both yeast extract and peptone (YP-grown P. spongiae) was highly inductive to larval settlement, whereas P. spongiae cells grown in the medium containing only peptone (P-grown P. spongiae) or YP-grown P. spongiae cells treated with chloramphenicol at the onset of biofilm development (YPC-grown P. spongiae) did not induce larval settlement. Analysis of biofilm formation, biofilm structure, and the surface protein profile indicated that only the induction-capable YP-grown P. spongiae formed a well-developed biofilm, while the P-grown P. spongiae and the YPC-grown P. spongiae did not. We report here for the first time that bacterial biofilm formation was associated with its induction of larval settlement.In the marine environment, natural and artificial substrata are readily colonized by micro-and macroorganisms in a process known as "biofouling" (4, 8, 52). The dioecious, freespawning, tube-building polychaete Hydroides elegans (Haswell 1883) is one of the most troublesome fouling organisms, occurring widely in tropical and subtropical seawaters (41, 51). Larval settlement of H. elegans marks the turning point from a planktonic life stage to a sessile life stage and represents a crucial step in biofouling. Factors affecting larval settlement are therefore the focus of biofouling studies and antifouling control.Competent larvae of H. elegans settled rapidly after induction by marine natural biofilms or certain monospecies bacterial films in the laboratory (26, 51). Larvae of H. elegans settle only in the presence of a metabolically active biofilm, however, not on a clean surface (21,27,51). Previous studies suggested that the bacterium-derived settlement cues were produced after bacteria attached to a surface and the cues were biofilm surface associated (11,13,19,25). However, little attention was paid as to whether the bacterial biofilm formation was involved in bacterial induction of larval settlement. Bacteria undergo profound changes in physiological features during biofilm formation, a dynamic process wherein bacteria transform from planktonic (free-swimming) organisms to cells that are part of a complex, surface-attached community (5,9,15,35,36,42,47). Recent research revealed that many kinds of bacterial activity, such as infection or symbioses and production of bioactive compounds, were associated with biofilm formation (2, 12, 32, 53). Microbiologists have turned to biofilm formation for explanations of interesting microbial behaviors/ bioactivities (37, 38).In this study, employing the newly described marine bacterium Pseudoalteromonas spongiae (24, 28), we investigated the possible relevance of biofilm formation for its ability to induce larval settlement of H. elegans.Effect of culture condition on bacterial induction of larval settlement. In...

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Adaptive responses to antimicrobial agents in biofilms

Cited by 120 publications

References 10 publications

Enhanced Benzaldehyde Tolerance in Zymomonas mobilis Biofilms and the Potential of Biofilm Applications in Fine-Chemical Production

Enhanced Benzaldehyde Tolerance in Zymomonas mobilis Biofilms and the Potential of Biofilm Applications in Fine-Chemical Production

Antimicrobial resistance, presence of integrons and biofilm formation ofSalmonellaPullorum isolates from eastern China (1962–2010)

Effect of Biofilm Formation by Pseudoalteromonas spongiae on Induction of Larval Settlement of the Polychaete Hydroides elegans

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