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Competitive inter-species interactions underlie the increased antimicrobial tolerance in multispecies brewery biofilms

The ISME Journalvolume 12pages20612075 (2018) | Download Citation

Abstract

Genetic diversity often enhances the tolerance of microbial communities against antimicrobial treatment. However the sociobiology underlying this antimicrobial tolerance remains largely unexplored. Here we analyze how inter-species interactions can increase antimicrobial tolerance. We apply our approach to 17 industrially relevant multispecies biofilm models, based on species isolated from 58 contaminating biofilms in three breweries. Sulfathiazole was used as antimicrobial agent because it showed the highest activity out of 22 biofilm inhibitors tested. Our analysis reveals that competitive interactions dominate among species within brewery biofilms. We show that antimicrobial treatment can reduce the level of competition and therefore cause a subset of species to bloom. The result is a 1.2–42.7-fold lower percentage inhibition of these species and increased overall tolerance. In addition, we show that the presence of Raoultella can also directly enhance the inherent tolerance of Pseudomonas to antimicrobial treatment, either because the species protect each other or because they induce specific tolerance phenotypes as a response to competitors. Overall, our study emphasizes that the dominance of competitive interactions is central to the enhanced antimicrobial tolerance of the multispecies biofilms, and that the activity of antimicrobials against multispecies biofilms cannot be predicted based on their effect against monocultures.

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Acknowledgements

We would like to thank S. Robijns, S. Van Puyvelde, and B. Lories for their valuable comments and for their assistance in sampling of brewery biofilms. We thank K. Deflem and D. De Coster for experimental assistance. This work was supported by the KU Leuven Research Fund (STG/16/022), by the Institute for the Promotion of Innovation through Science and Technology in Flanders under grant IWT-SBO 120050 (NEMOA) and by FWO-Vlaanderen (W0.009.16N). IP is a research assistant of the IWT-Vlaanderen (SB/131721). HPS acknowledges the receipt of a postdoctoral fellowship from FWO-Vlaanderen (PDO/11).

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  1. Department of Microbial and Molecular Systems, Centre of Microbial and Plant Genetics (CMPG), KU Leuven, Kasteelpark Arenberg 20 - box 2460, B-3001, Leuven, Belgium

    • Ilse Parijs
    •  & Hans P. Steenackers

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Correspondence to Hans P. Steenackers.

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https://doi.org/10.1038/s41396-018-0146-5