Quorum signaling mycotoxins: A new risk strategy for bacterial biocontrol of Fusarium verticillioides and other endophytic fungal species?

Authors: Bacon, Charles; Hinton, Dorothy; Mitchell, Trevor

Submitted to: Journal of Agricultural and Food Chemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/7/2016
Publication Date: 12/12/2016
Citation: Bacon, C.W., Hinton, D.M., Mitchell, T.R. 2016. Quorum signaling mycotoxins: A new risk strategy for bacterial biocontrol of Fusarium verticillioides and other endophytic fungal species? Journal of Agricultural and Food Chemistry. doi:10.1021/acs.jafc.6b03861.

Interpretive Summary: There are several biocontrol organisms used to prevent the infection and contamination of food and feed crops by fungi and their toxins. One broad class of organisms used for this purpose is microbial endophytes. These endophytes dwell within the spaces of plant roots, stems, and leaves, preventing infections by other pathogens. Bacterial endophytes are used as biocontrol organisms for plant pathogens such as the corn fungal endophyte Fusarium verticillioides and its subsequent production of fumonisin mycotoxins. However, such applications are not always predictable and efficient. All bacteria communicate via cell-dependent signals, which are referred to as quorum sensing resulting from metabolites that regulate gene expression that are effective in most instances of preventing infection with hopes of reducing mycotoxins accumulation. Since the intercellular spaces are the habitat for endophytes, it is expected that these spaces contain important signaling metabolites for numerous biochemical and morphological events that produce biocontrol efficiency. We hypothesize that quorum inhibitors and signals are produced by fungi for competitive purposes, altering the biocontrol efficiency of a competing biocontrol organism. Recently, quorum inhibitors have been isolated from several fungi, and three of these are mycotoxins. Biosensor bacteria are useful assays for detecting quorum sensing and inhibitory activities and we review our use and that of others as test of mycotoxins for quorum activity. Further, we present evidence of quorum quenching as means of developing control strategies, particularly as it relates to mycotoxic fungal endophytes, such as the Fusarium species.

Technical Abstract: Bacterial endophytes are used as biocontrol organisms for plant pathogens such as the maize endophyte Fusarium verticillioides and its production of fumonisin mycotoxins. However, such applications are not always predictable and efficient. All bacteria communicate via cell-dependent signals, which are referred to as quorum sensing resulting from metabolites that regulate gene expression. Since the intercellular spaces are the habitat for endophytes, it is expected that these spaces contain important signaling metabolites for numerous biochemical and morphological events that produce biocontrol efficiency. We hypothesize that quorum inhibitors are produced for competitive purposes, altering the biocontrol efficiency of a biocontrol organism. Recently, quorum inhibitors have been isolated from several fungi, and three of these are mycotoxins. Biosensor bacteria are useful assays for both quorum sensing and inhibitory activities and we review their use as test of mycotoxins for quorum activity. We test other mycotoxins, including the fumonisin mycotoxins, for quorum activity using the biosensor bacteria. We scored each of the nine tested mycotoxins for quorum activity, and discussed their activity along with reviews on quorum quenching and its regulation as means of developing control strategies, particularly as it relates to mycotoxic fungal endophytes, such as the Fusarium species.