Abstract
Microorganisms release a plethora of volatile secondary metabolites. Up to now, it has been widely accepted that these volatile organic compounds are produced and emitted as a final product by a single organism e.g. a bacterial cell. We questioned this commonly assumed perspective and hypothesized that in diversely colonized microbial communities, bacterial cells can passively interact by emitting precursors which non-enzymatically react to form the active final compound. This hypothesis was inspired by the discovery of the bacterial metabolite schleiferon A. This bactericidal volatile compound is formed by a non-enzymatic reaction between acetoin and 2-phenylethylamine. Both precursors are released by Staphylococcus schleiferi cells. In order to provide evidence for our hypothesis that these precursors could also be released by bacterial cells of different species, we simultaneously but separately cultivated Serratia plymuthica 4Rx13 and Staphylococcus delphini 20771 which held responsible for only one precursor necessary for schleiferon A formation, respectively. By mixing their headspace, we demonstrated that these two species were able to deliver the active principle schleiferon A. Such a joint formation of a volatile secondary metabolite by different bacterial species has not been described yet. This highlights a new aspect of interpreting multispecies interactions in microbial communities as not only direct interactions between species might determine and influence the dynamics of the community. Events outside the cell could lead to the appearance of new compounds which could possess new community shaping properties.
Highlights
Microorganisms release a plethora of volatile secondary metabolites
We could search for an acetoin producing bacterial strain that would not be able to emit 2-phenylethylamine and vice versa a bacterial isolate that emits solely 2-phenylethylamine
Our experiments strongly indicate that in a microbial community volatile products can arise from microbial precursor molecules which originate from cells of different species
Summary
Microorganisms release a plethora of volatile secondary metabolites. Up to now, it has been widely accepted that these volatile organic compounds are produced and emitted as a final product by a single organism e.g. a bacterial cell. We questioned this commonly assumed perspective and hypothesized that in diversely colonized microbial communities, bacterial cells can passively interact by emitting precursors which non-enzymatically react to form the active final compound This hypothesis was inspired by the discovery of the bacterial metabolite schleiferon A. In order to provide evidence for our hypothesis that these precursors could be released by bacterial cells of different species, we simultaneously but separately cultivated Serratia plymuthica 4Rx13 and Staphylococcus delphini 20771 which held responsible for only one precursor necessary for schleiferon A formation, respectively By mixing their headspace, we demonstrated that these two species were able to deliver the active principle schleiferon A. These species a priori have the potential to synthesize precursors of final volatile products This fueled the hypothesis that precursors like acetoin or 2-phenylethylamine released by different species into the headspace of a microbial community will spontaneously react to non-enzymatically form an active principle like schleiferon A (and B). This mechanism could contribute besides direct microbial interactions to a variable composition of the headspace and adds a new aspect to the in generally known dynamics of microbial communities
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