Fungal volatile compounds induce production of the secondary metabolite Sodorifen in Serratia plymuthica PRI-2C

Abstract

The ability of bacteria and fungi to communicate with each other is a remarkable aspect of the microbial world. It is recognized that volatile organic compounds (VOCs) act as communication signals, however the molecular responses by bacteria to fungal VOCs remain unknown. Here we perform transcriptomics and proteomics analyses of Serratia plymuthica PRI-2C exposed to VOCs emitted by the fungal pathogen Fusarium culmorum. We find that the bacterium responds to fungal VOCs with changes in gene and protein expression related to motility, signal transduction, energy metabolism, cell envelope biogenesis, and secondary metabolite production. Metabolomic analysis of the bacterium exposed to the fungal VOCs, gene cluster comparison, and heterologous co-expression of a terpene synthase and a methyltransferase revealed the production of the unusual terpene sodorifen in response to fungal VOCs. These results strongly suggest that VOCs are not only a metabolic waste but important compounds in the long-distance communication between fungi and bacteria.Interactions and communication among organisms are central to understanding any ecosystem. The essential role of volatile organic compounds (VOCs) in the communication with other organisms, also known as infochemicals, has been acknowledged for more than 30 years 1 . However, their ecological functions have been mainly studied for aboveground plant-plant and plant-insect interactions 2, 3 . In recent years, VOCs are becoming increasingly important in the field of microbial ecology. Due to their unique nature (low molecular mass, high vapor pressure, low boiling point and a lipophilic moiety) VOCs play important roles in the long-distance interactions and communication within the microbial world 4 . In soil and in the rhizosphere, VOCs readily diffuse under atmospheric pressure and travel throughout the abundant air-and liquid-filled pockets of the soil 4, 5 .Several soil-associated bacteria were shown to have positive effects on plant growth and resistance 6-8 , as well as to have the ability to control plant diseases via production of VOCs 9 . Various studies have documented that VOCs can have diverse roles in the interaction between physically separated microorganisms, ranging from infochemical molecules affecting the behavior, population dynamics and gene expression in responding microorganisms to interference competition tools suppressing or eliminating potential enemies 4, 10-13 . Interestingly, most studies have only examined the role of bacterial VOCs and their effect on plants and fungi. However, the role and function of fungal VOCs on bacteria remains largely unknown. Only few studies demonstrated that the growth of some bacterial species was suppressed by fungal VOCs 14 . For example, VOCs produced by the oyster mushroom Pleurotus ostreatus showed inhibitory effects on Bacillus cereus and Bacillus subtilis 15 . Another study by Lutz et al. 16 demonstrated that VOCs emitted by T. atroviride increased the expression of a biocontrol gene (phlA) of P. fluorescens.Previous...

Airborne medicine: bacterial volatiles and their influence on plant health

“…The 'smell' or 'volatilome' of a given bacterial strain is usually constituted of a wide diversity of volatile compounds, whose composition and relative abundance change with growth phase or growth conditions (Kai et al, 2010;Blom et al, 2011a). Recent work indicates that the emission of particular volatiles can be induced by the presence of interacting partners (Schmidt et al, 2017), suggesting complex regulation of the synthesis and/or emission of these metabolites rather than unspecific release of 'metabolic waste products'. In general, closely related strains emit more similar volatilomes than phylogenetically more distant strains do (Ryu et al, 2003;Kai et al, 2007;Groenhagen et al, 2013).…”

Interkingdom microbial consortia mechanisms to guide biotechnological applications

“…1E). For example, volatile organic compounds produced by the fungus Fusarium culmorum induced the expression of a wide range of genes and proteins from the bacterium Serratia plymuthica including the production of a previously unknown terpene sodorifen that may play a role in fungal-bacterial long-distance communication (Schmidt et al, 2017). In consortia containing fungi and bacteria (or algae), fungi often act as 'dispersion vectors' for others, increasing nutrient availability and providing physical protection.…”

The ecological role of volatile mediated interactions belowground

“…Recently, it was demonstrated that those VOCs play an important role in the long-distance interaction with bacteria by affecting both motility and production of secondary metabolites (Schmidt et al 2016;Schmidt et al 2017). Here, VOCs of F. culmorum did not significantly stimulated bacterial motility and function as repellence as in the case of Burkholderia or Janthinobacterium.…”

“…Exposure to microbial VOCs can lead to global transcriptomic changes of soil microbes (Yung et al, 2015;Schmidt et al 2017). However, as indicated in Chapter 2 the perception of VOCs is largely unknown.…”