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Biofilm formation as an extra gear for Apilactobacillus kunkeei to counter the threat of agrochemicals in honeybee crop - PubMed

Biofilm formation as an extra gear for Apilactobacillus kunkeei to counter the threat of agrochemicals in honeybee crop

Ali Zein Alabiden Tlais et al. Microb Biotechnol. 2022 Aug.

Abstract

The alteration of a eubiosis status in honeybees' gut microbiota is directly linked to the occurrence of diseases, and likely to the honeybees decline. Since fructophilic lactobacilli were suggested as symbionts for honeybees, we mechanistically investigated their behaviour under the exposure to agrochemicals (Roundup, Mediator and Reldan containing glyphosate, imidacloprid and chlorpyrifos-methyl as active ingredients respectively) and plant secondary metabolites (nicotine and p-coumaric acid) ingested by honeybees as part of their diet. The effects of exposure to agrochemicals and plant secondary metabolites were assessed both on planktonic cells and sessile communities of three biofilm-forming strains of Apilactobacillus kunkeei. We identified the high sensitivity of A. kunkeei planktonic cells to Roundup and Reldan, while cells embedded in mature biofilms had increased resistance to the same agrochemicals. However, agrochemicals still exerted a substantial inhibitory/control effect if the exposure was during the preliminary steps of biofilm formation. The level of susceptibility resulted to be strain-specific. Exopolysaccharides resulted in the main component of extracellular polymeric matrix (ECM) in biofilm, but the exposure to Roundup caused a change in ECM production and composition. Nicotine and p-coumaric acid had a growth-promoting effect in sessile communities, although no effect was found on planktonic growth.

© 2022 The Authors. Microbial Biotechnology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig. 1
Fig. 1

Growth kinetics (Ab620) of Aplilactobacillus kunkeei BEE4, BV61 and PL13 under exposure to plant secondary metabolites (nicotine and p‐coumaric acid) and agrochemicals (Mediator, Reldan and Roundup) for 24 h at 30°C. Data are the mean of three separate analyses ± standard deviations.

Fig. 2
Fig. 2

Confocal microscopy analysis of biofilms by Apilactobacillus kunkeei BEE4 (panels A–F), BV61 (G–L) and PL13 (M–R) that were exposed, after grown, to nicotine (panels B, H, N), p‐coumaric acid (C, I, O), Mediator (D, J, P), Reldan (E, K, Q) and Roundup (F, L, R). Panels A, G, M represent control biofilms without exposure to agrochemicals or plant secondary metabolites. Bacterial cells show green fluorescence and exopolysaccharides in biofilm extracellular polymeric matrix show red fluorescence. Scale bars represent 100 μm; units of x, y and z axes are μm.

Fig. 3
Fig. 3

Cell density (Log CFU g−1) (A) and biomass (mg) (B) of Apilactobacillus kunkeei BEE4, BV61 and PL13 biofilms that, after 96 h of growth, were exposed to various plant secondary metabolites (nicotine and p‐coumaric acid) and agrochemicals (Mediator, Reldan and Roundup). ‘Control’ indicates the control sample without supplementation of phytosanitary products and plant secondary metabolites. Data are the mean of three separate analyses ± standard deviations. Bars with different superscript letters differ significantly (P < 0.05).

Fig. 4
Fig. 4

Apilactobacillus kunkeei BEE4, BV61 and PL13 biofilms after 96 h of growth under exposure to various plant secondary metabolites (nicotine and p‐coumaric acid) and agrochemicals (Mediator, Reldan and Roundup). Control indicates the control sample without supplementation of phytosanitary products and plant secondary metabolites.

Fig. 5
Fig. 5

Confocal microscopy analysis of biofilms produced by Apilactobacillus kunkeei BEE4 (panels A–F), BV61 (G–L) and PL13 (M–R) under exposure to nicotine (panels B, H, N), p‐coumaric acid (C, I, O), Mediator (D, J, P), Reldan (E, K, Q) and Roundup (F, L, R). Panels A, G, M represent control biofilms without exposure to agrochemicals or plant secondary metabolites. Bacterial cells show green fluorescence and EPS in biofilm ECM show red fluorescence. Scale bars represent 50 μm; units of x, y and z axes are μm.

Fig. 6
Fig. 6

Cell density (Log CFU g−1) (A), biomass (mg) (B) and relative abundance of different extracellular polymeric matrix components (C) of Apilactobacillus kunkeei BEE4, BV61 and PL13 biofilms after 96 h of growth under exposure to various plant secondary metabolites (nicotine and p‐coumaric acid) and agrochemicals (Mediator, Reldan and Roundup). ‘Control’ indicates the control sample without supplementation of phytosanitary products and plant secondary metabolites. Data are the mean of three separate analyses ± standard deviations. Bars with different superscript letters differ significantly (P < 0.05).

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