Biofilm parameters influencing biocide efficacy

Srinivasan, Rohini; Stewart, Philip S.; Griebe, Thomas; Chen, Ching-I; Xu, Xiaoming

doi:10.1002/bit.260460608

Cited by 57 publications

(22 citation statements)

References 23 publications

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“…Conversely, the deposition of calcite particles onto the biofilm surface hindered solute transport and decreased chlorine killing. The latter observation is consistent with the findings of a previous study showing that the deposition of calcite and clay particles decreased the susceptibility of biofilms to biocides (36). Further, we previously observed that in situ biomineralization of calcite occurs throughout the biofilm, while abiotically precipitated particles deposit onto the biofilm surface (29).…”

Section: Discussionsupporting

confidence: 93%

In Situ Biomineralization and Particle Deposition Distinctively Mediate Biofilm Susceptibility to Chlorine

Chopp

Russin

et al. 2016

Appl Environ Microbiol

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Microbial biofilms and mineral precipitation commonly co-occur in engineered water systems, such as cooling towers and water purification systems, and both decrease process performance. Microbial biofilms are extremely challenging to control and eradicate. We previously showed that in situ biomineralization and the precipitation and deposition of abiotic particles occur simultaneously in biofilms under oversaturated conditions. Both processes could potentially alter the essential properties of biofilms, including susceptibility to biocides. However, the specific interactions between mineral formation and biofilm processes remain poorly understood. Here we show that the susceptibility of biofilms to chlorination depends specifically on internal transport processes mediated by biomineralization and the accumulation of abiotic mineral deposits. Using injections of the fluorescent tracer Cy5, we show that Pseudomonas aeruginosa biofilms are more permeable to solutes after in situ calcite biomineralization and are less permeable after the deposition of abiotically precipitated calcite particles. We further show that biofilms are more susceptible to chlorine killing after biomineralization and less susceptible after particle deposition. Based on these observations, we found a strong correlation between enhanced solute transport and chlorine killing in biofilms, indicating that biomineralization and particle deposition regulate biofilm susceptibility by altering biocide penetration into the biofilm. The distinct effects of in situ biomineralization and particle deposition on biocide killing highlight the importance of understanding the mechanisms and patterns of biomineralization and scale formation to achieve successful biofilm control.T he development of biofilms in engineered water systems is usually detrimental. Excessive biofilm growth decreases process performance; for example, it reduces the heat exchange efficiency in cooling towers and hinders the flow through high-pressure water treatment membranes (1, 2). Biofilms in water systems are also potential reservoirs of human pathogens (2-6). Biofilms are difficult to eradicate because they are much less susceptible to antimicrobials and biocides than suspended microbial cells (7,8). The decreased susceptibility of biofilms to biocides results from a combination of the decreased penetration of solutes into the biofilm structure, the protection provided by extracellular polymers, reduced cellular metabolism within biofilms, and the development of resistant cellular phenotypes (persisters) (9-11). Chlorine is one of the most commonly used biocides for biofilm control in engineered water systems (12, 13). Prior studies have found that the limited transport of chlorine to the interior of biofilms reduces the overall killing efficacy of chlorination (12,14).Biofilm biofouling is often associated with the formation of scale, which is an inorganic mineral precipitate that commonly includes calcium carbonate, sulfate, and phosphate (1, 15, 16). The co-occurrence of a biofi...

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Section: Discussionsupporting

confidence: 93%

In Situ Biomineralization and Particle Deposition Distinctively Mediate Biofilm Susceptibility to Chlorine

Chopp

Russin

et al. 2016

Appl Environ Microbiol

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“…This indicates that specific bacterial subpopulations may occur, persist and spread within the systems as demonstrated for staphylococci by PFGE. Such observations indicate the possibility that these bacteria may survive in biofilm communities (Sharma & Anand 2002), in which increased levels of resistance to disinfectants have been recorded (Brooks & Flint 2008), and where the disinfectant efficacy could be adversely affected by the cell population density (Srinivasan et al 1995). e. coli, which was rarely found on the inside surfaces, originated mainly from such highly contaminated surface sites.…”

Section: Discussionmentioning

confidence: 93%

Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants

Schlegelová¹,

Babák²,

Holasová³

et al. 2010

Czech J. Food Sci.

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Schlegelová J., Babák V., Holasová M., Konstantinová L., Necidová L., Šišák F., Vlková H., Roubal P., Jaglic Z. (2010): Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants. Czech J. Food Sci., 28: 450-461.The occurrence of listeria monocytogenes, Salmonella spp., Bacillus cereus, Staphylococcus spp., enterococcus spp., and escherichia coli in raw food materials, food products, and on food contact surfaces after sanitation was investigated during the period of 2005-2006 in three dairy cattle farms (120 samples), one dairy (124 samples), and two meat processing plants (160 samples). A total of 1409 isolates were identified. The epidemiological characterisation and determination of the virulence factors and antimicrobial resistance were performed on selected isolates. The level of bacterial contamination generally decreased during the production process (the contamination of food products was lower than that of raw material). However, the contamination of food contact surfaces was relatively high even after sanitation. Moreover, specific microbiological profiles were found on the inside equipment surfaces in dairy facilities, where genetically closely related multi-resistant strains persisting in biofilm communities may occur as demonstrated for staphylococci. Although the occurrence of potentially significant pathogens was not high, the microorganisms such as l. monocytogenes, Salmonella spp., and shiga-toxin positive e. coli principally contaminated the meat processing plants. B. cereus isolates, among which 76% were positive for diarrhogenic enterotoxin, typically occurred on the inside equipment surfaces and in the heat-treated products.

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“…Prior studies have found that deposition of solid particles alters biofilm morphology (43,44). It has been suggested that this process should increase biofilm resistance to biocides by reducing transport of solutes into and within biofilms (45), but this hypothesis has not been tested experimentally. Calcium carbonate precipitation has also been found to increase the rigidity and strength of aerobic granules, which are biofilm-like suspended aggregates of cells encased in a matrix (21).…”

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confidence: 99%

Spatial Patterns of Carbonate Biomineralization in Biofilms

Chopp

Russin

et al. 2015

Appl Environ Microbiol

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dMicrobially catalyzed precipitation of carbonate minerals is an important process in diverse biological, geological, and engineered systems. However, the processes that regulate carbonate biomineralization and their impacts on biofilms are largely unexplored, mainly because of the inability of current methods to directly observe biomineralization within biofilms. Here, we present a method for in situ, real-time imaging of biomineralization in biofilms and use it to show that Pseudomonas aeruginosa biofilms produce morphologically distinct carbonate deposits that substantially modify biofilm structures. The patterns of carbonate biomineralization produced in situ were substantially different from those caused by accumulation of particles produced by abiotic precipitation. Contrary to the common expectation that mineral precipitation should occur at the biofilm surface, we found that biomineralization started at the base of the biofilm. The carbonate deposits grew over time, detaching biofilm-resident cells and deforming the biofilm morphology. These findings indicate that biomineralization is a general regulator of biofilm architecture and properties. Microbially induced carbonate precipitation represents an essential pathway for sequestration of large amounts of carbon in ancient and modern environments (1-5). Rock records reveal that Precambrian stromatolites formed as a consequence of trapping, binding, and precipitation of calcium carbonate by the growth and metabolism of microorganisms (2-4). Modern carbonate microbialites are found in a wide range of environments, including freshwater, oceans, hypersaline lakes, and soils (6, 7). Clinically, prolonged bacterial infection of indwelling urinary catheters leads to the formation of mineralized biofilms that can occlude the catheter lumen and cause serious complications (8-10). Some persistent infections of the lungs, particularly those associated with the genetic disorder primary ciliary dyskinesia, involve precipitation of calcium-rich stones or coatings (11)(12)(13)(14). In engineered systems, microbially induced scale formation decreases the performance of a wide variety of processes, including membrane separations in water treatment and heat exchange efficiency in cooling towers (15, 16). More recently, calcium carbonate biomineralization has also been explored as a novel biotechnology for the purpose of bioremediation and stabilization of porous structures, including soils, sediments, and construction materials (17-21).The microorganisms involved in carbonate biomineralization cover nearly all classes, including bacteria, algae, and fungi (22-27). It has been reported that more than 200 soil bacteria, including Pseudomonas spp., Bacillus subtilis, and Azotobacter spp., are capable of inducing calcium carbonate precipitation (5). Diverse microbial metabolisms, such as photosynthesis, sulfate reduction, and urea hydrolysis, can induce carbonate precipitation by significantly changing the saturation state of calcium carbonate (28,29). Microbial respiration p...

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Biofilm parameters influencing biocide efficacy

Cited by 57 publications

References 23 publications

In Situ Biomineralization and Particle Deposition Distinctively Mediate Biofilm Susceptibility to Chlorine

In Situ Biomineralization and Particle Deposition Distinctively Mediate Biofilm Susceptibility to Chlorine

Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants

Spatial Patterns of Carbonate Biomineralization in Biofilms

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