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

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 (MK) 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 MK 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 MK 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.

Identification and Functional Characterization of a Soybean (Glycine max) Thioesterase that Acts on Intermediates of Fatty Acid Biosynthesis

“…The 2-methylketones, primarily 2-undecanone and 2-tridecanone, from wild tomatoes act as natural insecticides [11]. Although the biological function of ShMKS2 homologs in other plant species remains to be elucidated, there is cumulative evidence that suggests a defensive role for MKS2/ALT-like proteins in those plants [10,17,19,29]. In eggplants, artificial wounding, methyl jasmonate (MeJA) treatment, or methyl salicylate (MeSA) treatment upregulated the transcriptional expression of SmMKS2-1 gene in the leaves [29].…”

“…In Arabidopsis, herbivore-damaged plants emitted more 2-pentanone than undamaged plants [36]. In addition to the protective role against herbivorous insects, 2-tridecanone can also affect surface mobility and biofilm formation of both pathogenic and symbiotic bacteria and as a result, interfere with the bacterial colonization of plant roots [19]. In this study, we also observed that the main transcript of GmMKS2 , GmMKS2-X2 , was universally present in all tissues examined, but its expression was the highest in the roots.…”

“…Recently, 2-tridecanone and other medium-chain 2-methylketones have been demonstrated to act as chemical cues that affect bacterial behavior on surfaces and hinder plant–bacteria interactions. Notably, the application of 2-tridecanone interfered not only with the pathogenic interaction between a bacterium and its plant host but also with the symbiotic Rhizobium –legume interaction [19]. Searches in the database have revealed that G. max possesses only one MKS2 / ALT -like gene, but expression in Escherichia coli of a chemically synthesized gene for the GmALT failed to show any thioesterase activity of this protein [12], possibly because an inactive alternative-splicing sequence was used (see below).…”

Rhizobial Volatiles: Potential New Players in the Complex Interkingdom Signaling With Legumes

“…In rhizobia, QS usually relies on the production and perception of N-acyl-homoserine lactones (AHLs) that control important functions, some of which are relevant for the interaction with the legume host (Calatrava-Morales et al, 2018). Strigolactones (SLs), a group of carotenoid-derived plant hormones exuded by roots, participate in the interaction of plants with beneficial soil microorganisms (López-Ráez et al, 2017).…”

Role of Sinorhizobium meliloti and Escherichia coli Long-Chain Acyl-CoA Synthetase FadD in Long-Term Survival

“…However, the accumulation of free fatty acids was not responsible for the swarming phenotype observed in a S. meliloti fadD-mutant. Instead, the fadD-associated swarming phenotype was due to increased formation of the volatile 2-tridecanone [4].…”