The effect of Sinorhizobium meliloti volatilomes and synthetic long-chain methylketones on soil and Medicago truncatula microbiomes

Bacterial volatile compounds play important roles in intra- and interkingdom interactions but very little is known about their effects on soil and plant microbiomes. The legume symbiont Sinorhizobium meliloti (Sm) releases volatile methylketones (MKs), one of which acts as an infochemical in bacteria and hampers plant-bacteria interactions. MK production in Sm is modestly increased in the absence of the long-chain-fatty-acyl-coenzyme-A (CoA) synthetase FadD. To explore further the ecological role of MKs on soil and plant bacterial communities, we aimed at obtaining an MK-overproducer Sm strain by deleting the 3-oxo-acyl-CoA-thiolase-encoding fadA gene. Analyses of the Sm wild type (wt), and fad mutant volatilomes identified seventeen compounds consisting mostly of MKs and fatty acid methyl esters (FAMEs) and revealed that the fadA mutant produced more MKs than the fadD mutant and much more than the wt, while in the fadD mutant FAME emission was increased. When natural soil or the rhizosphere of Medicago truncatula were exposed to wt and fadA volatilomes or synthetic MKs, bacterial alpha- or beta-diversity were not strongly affected but specific genera were identified which responded differentially to each condition. Interestingly, Sm volatilomes had a significant effect on root endosphere Ensifer/Sinorhizobium populations by maintaining their abundance over time in contrast to control conditions or exposure to synthetic MKs. This study provides new insights on the synthesis of rhizobial volatile compounds and represents the first exploration of the effects of bacterial volatilomes on plant bacterial communities, contributing to increase our knowledge on the complex molecular bases underlying plant-bacteria interactions.