Synthesis and Biological Evaluation of the Novel Growth Inhibitor Streptol Glucoside, Isolated from an Obligate Plant Symbiont

Abstract

The plant Psychotria kirkii hosts an obligatory bacterial symbiont, Candidatus Burkholderia kirkii, in nodules on their leaves. Recently, a glucosylated derivative of (+)-streptol, (+)-streptol glucoside, was isolated from the nodulated leaves and was found to possess a plant growth inhibitory activity. To establish a structure-activity relationship study, a convergent strategy was developed to obtain several pseudosugars from a single synthetic precursor. Furthermore, the glucosylation of streptol was investigated in detail and conditions affording specifically the or glucosidic anomer were identified. Although (+)-streptol was the most active compound, its concentration in P. kirkii plant leaves extract was approximately tenfold lower than that of (+)-streptol glucoside. These results provide compelling evidence that the glucosylation of (+)-streptol protects the plant host against the growth inhibitory effect of the compound, which might constitute a molecular cornerstone for this successful plant-bacteria symbiosis.

Is the bacterial leaf nodule symbiosis obligate for Psychotria umbellata? The development of a Burkholderia-free host plant

“…In addition to kirkamide, other glucosides, such as streptol glucoside, were identified in P . punctata [28,34,66,68]. Streptol glucoside has been shown to inhibit germination of lettuce seeds, which could give the host an allelopathic advantage [66,68].…”

“…punctata [28,34,66,68]. Streptol glucoside has been shown to inhibit germination of lettuce seeds, which could give the host an allelopathic advantage [66,68]. Although we did not investigate functional pathways within our study to support one of these hypotheses, the growth difference in a controlled nutrient-rich environment (and in absence of any herbivores) suggests that benefits of the bacterial leaf nodulation are not solely ameliorating the host’s defence.…”

Induction of antibiotic specialized metabolism by co‐culturing in a collection of phyllosphere bacteria

“…The sampling of previously underexplored ecosystems has in turn led to the discovery of novel lipodepsipeptides and darobactin from insect microbiomes (Ganley et al ., 2018; Imai et al ., 2019), lobatamides from a plant symbiont (Ueoka et al ., 2020), or lugdunin from the human gut microbiota (Zipperer et al ., 2016). Inspired by these studies, and our own realization that specialized metabolism forms the basis of several obligate bacterial leaf symbioses (Sieber et al ., 2015; Carlier et al ., 2016; Pinto‐Carbó et al ., 2016, 2018; De Meyer et al ., 2019; Hsiao et al ., 2019), we hypothesized that the above‐ground surfaces of plants could provide rich and underexplored opportunities for the discovery of novel bioactive metabolites. The phyllosphere in particular hosts taxonomically diverse communities and harbours a majority of culturable taxa (Kinkel, 1997; Whipps et al ., 2008; Bai et al ., 2015; Massoni et al ., 2019).…”

Early steps in the evolution of vertical transmission revealed by a plant-bacterium symbiosis

“…We have previously shown that more than 10% of the proteome of Ca . Burkholderia kirkii , the obligate symbiont of Psychotria kirkii , was dedicated to the synthesis of cyclitol compounds with insecticidal an herbicidal properties [69, 70]. Similarly, the leaf nodule symbiont of Ardisia crenata synthesizes FR900359, a depsipeptide inhibitor of mammalian Gq proteins and potent insecticide [10, 14].…”