Environmental Dissolved Organic Matter Governs Biofilm Formation and Subsequent Linuron Degradation Activity of a Linuron-Degrading Bacterial Consortium

Abstract

It was examined whether biofilm growth on dissolved organic matter (DOM) of a three-species consortium whose members synergistically degrade the phenylurea herbicide linuron affected the consortium's integrity and subsequent linuron-degrading functionality. Citrate as a model DOM and three environmental DOM (eDOM) formulations of different quality were used. Biofilms developed with all DOM formulations, and the three species were retained in the biofilm. However, biofilm biomass, species composition, architecture, and colocalization of member strains depended on DOM and its biodegradability. To assess the linuron-degrading functionality, biofilms were subsequently irrigated with linuron at 10 mg liter ؊1 or 100 g liter ؊1 . Instant linuron degradation, the time needed to attain maximal linuron degradation, and hence the total amount of linuron removed depended on both the DOM used for growth and the linuron concentration. At 10 mg liter ؊1 , the final linuron degradation efficiency was as high as previously observed without DOM except for biofilms fed with humic acids which did not degrade linuron. At 100 g liter ؊1 linuron, DOM-grown biofilms degraded linuron less efficiently than biofilms receiving 10 mg liter ؊1 linuron. The amount of linuron removed was more correlated with biofilm species composition than with biomass or structure. Based on visual observations, colocalization of consortium members in biofilms after the DOM feed appears essential for instant linurondegrading activity and might explain the differences in overall linuron degradation. The data show that DOM quality determines biofilm structure and composition of the pesticide-degrading consortium in periods with DOM as the main carbon source and can affect subsequent pesticide-degrading activity, especially at micropollutant concentrations. P esticides are applied worldwide in agriculture to ensure food production and safety but form a threat as contaminants in soil, groundwater, and surface water. Biodegradation is an important process in the attenuation of pollution by pesticides. For some pesticides, bacteria containing specialized metabolic pathways for mineralization and usage of the pesticides as the sole carbon and energy source have been identified (1, 2). Pesticide mineralization is achieved by either single strains or mixed-species consortia. In the latter, pesticides are converted to mineral components through synergistic metabolic interactions between the members (3, 4). Often such synergistic interactions manifest themselves in the formation of mixed-species aggregates and biofilms in suspended cultures and on solid surfaces, respectively (5, 6).In the environment, pesticides form an unreliable carbon source with concentrations that show large temporal and spatial variability (7) and that are often in the micropollutant range, i.e., in the picogram liter Ϫ1 and microgram liter Ϫ1 range (8). Instead, natural dissolved organic matter (DOM) provides the most important carbon and energy source for heterotrophic bacteria (9-11). This im...

Biofilm formation of a bacterial consortium on linuron at micropollutant concentrations in continuous flow chambers and the impact of dissolved organic matter

“…When afterward linuron was supplied together with the other C‐sources, WDL7‐Rfp returned. This agrees with a previous study in which the consortium's integrity, for example, the presence of strains WDL7‐Rfp and WDL1, remained when the consortium, after inoculation, was directly grown as a biofilm on DOM/citrate without linuron in the feed (Horemans et al ., ). This is explained by the earlier observation of synergism between consortium members during eDOM degradation (Horemans et al ., ) and single C‐substrates (Horemans et al ., ).…”

“…Interestingly, the consortium members appear also to interact in the degradation of DOM of environmental origin (eDOM) (Horemans et al, 2013b) of various quality and of various single carbon substrates besides linuron (Horemans et al, 2013a). Such interactions were observed to counteract detrimental effects of auxiliary carbon sources on linuron degradation in continuous biofilms as the integrity of the consortium was ensured (Horemans et al, 2013d). In a recent study, we examined the effects of DOM quality on linuron degradation by the consortium biofilms in continuous flow chamber systems that were continuously fed with DOM and linuron simultaneously at relatively high linuron concentrations (Horemans et al, 2013e).…”

Better together: engineering and application of microbial symbioses

“…In bioremediation, which repurposes or engineers organisms to clean up pollutants, division of labor is crucial because complex toxic compounds often require several steps for degradation and cultures must be robust to whatever compounds are present making microbial communities and ideal solution. [65][66][67][68][69][70][71] Petroleum can be degraded naturally by consortia that produce biosurfactants which make hydrocarbons accessible through emulsification. [69] Mnif et al successfully mimicked this concept synthetically by pairing a three-microbe degradation consortium with surfactant producing strains of Bacillus subtilis and Acinetobacter radioresistens.…”

Substratum‐Associated Microbiota

“…Direct electron transfer between electrochemically "selected" bacteria and cathodes may be involved in efficient denitrification and would contribute to improve denitrification efficiency. Horemans et al (2013) found that the amount of the phenylurea herbicide linuron removed in a linorum degrading bacteria consortium correlated more with biofilm species composition than with biomass or structure. Atashgahi et al (2013) bathing areas must be classified as "contaminated" or "highly contaminated".…”