2-Tridecanone impacts surface-associated bacterial behaviours and hinders plant-bacteria interactions

López-Lara, Isabel M.; Nogales, Joaquina; Pech-Canul, Angel; Calatrava-Morales, Nieves; Bernabéu-Roda, Lydia M.; Durán, Paoloma; Cuéllar, Virginia; Olivares, José; Alvarez, Laura; Palenzuela-Bretones, Diana; Romero, Manuel; Heeb, Stephan; Cámara, Miguel; Geiger, Otto; Soto, Maria J.

Abstract

Surface motility and biofilm formation are behaviours which enable bacteria to infect their hosts and are controlled by different chemical signals. In the plant symbiotic alpha‐proteobacterium Sinorhizobium meliloti, the lack of long‐chain fatty acyl‐coenzyme A synthetase activity (FadD) leads to increased surface motility, defects in biofilm development, and impaired root colonization. In this study, analyses of lipid extracts and volatiles revealed that a fadD mutant accumulates 2‐tridecanone (2‐TDC), a methylketone known as a natural insecticide. Application of pure 2‐TDC to the wild‐type strain phenocopies the free‐living and symbiotic behaviours of the fadD mutant. Structural features of the methylketone determine its ability to promote S. meliloti surface translocation, which is mainly mediated by a flagella‐independent motility. Transcriptomic analyses showed that 2‐TDC induces differential expression of iron uptake, redox, and stress‐related genes. Interestingly, this methylketone also influences surface motility and impairs biofilm formation in plant and animal pathogenic bacteria. Moreover, 2‐TDC not only hampers alfalfa nodulation but also the development of tomato bacterial speck disease. This work assigns a new role to 2‐TDC as an infochemical that affects important bacterial traits and hampers plant‐bacteria interactions by interfering with microbial colonization of plant tissues.

Citation

López-Lara, I. M., Nogales, J., Pech-Canul, A., Calatrava-Morales, N., Bernabéu-Roda, L. M., Durán, P., Cuéllar, V., Olivares, J., Alvarez, L., Palenzuela-Bretones, D., Romero, M., Heeb, S., Cámara, M., Geiger, O., & Soto, M. J. (2018). 2-Tridecanone impacts surface-associated bacterial behaviours and hinders plant-bacteria interactions. Environmental Microbiology, 20(6), 2049-2065. https://doi.org/10.1111/1462-2920.14083

• Journal Article Type: Article
• Acceptance Date: Feb 23, 2018
• Online Publication Date: Feb 28, 2018
• Publication Date: Jun 1, 2018
• Deposit Date: Feb 26, 2018
• Publicly Available Date: Mar 1, 2019
• Journal: Environmental Microbiology
• Print ISSN: 1462-2912
• Electronic ISSN: 1462-2920
• Publisher: Wiley
• Peer Reviewed: Peer Reviewed
• Volume: 20
• Issue: 6
• Pages: 2049-2065
• DOI: https://doi.org/10.1111/1462-2920.14083
• Public URL: https://nottingham-repository.worktribe.com/output/917372
• Publisher URL: https://onlinelibrary.wiley.com/doi/abs/10.1111/1462-2920.14083
• Additional Information: This is the peer reviewed version of the following article: López-Lara, I. M., Nogales, J. , Pech-Canul, Á. , Calatrava-Morales, N. , Bernabéu-Roda, L. M., Durán, P. , Cuéllar, V. , Olivares, J. , Alvarez, L. , Palenzuela-Bretones, D. , Romero, M. , Heeb, S. , Cámara, M. , Geiger, O. and Soto, M. J. (2018), 2-Tridecanone impacts surface-associated bacterial behaviours and hinders plant–bacteria interactions. Environmental Microbiology doi:10.1111/1462-2920.14083, which has been published in final form at https://doi.org/10.1111/1462-2920.14083. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.
• Contract Date: Feb 26, 2018