Ecological implications of hypoxia‐triggered shifts in secondary metabolism

Abstract

Summary Members of the actinomycete genus Streptomyces are non-motile, filamentous bacteria that are well known for the production of biomedically relevant secondary metabolites. While considered obligate aerobes, little is known about how these bacteria respond to periods of reduced oxygen availability in their natural habitats, which include soils and ocean sediments. Here we provide evidence that the marine streptomycete strain CNQ-525 can reduce MnO2 via a diffusible mechanism. We investigated the effects of hypoxia on secondary metabolite production and observed a shift away from the antibiotic napyradiomycin towards 8-amino-flaviolin, an intermediate in the napyradiomycin biosynthetic pathway. We purified 8-amino-flaviolin and demonstrated that it is reversibly redox-active (midpoint potential –474.5 mV), indicating that it has the potential to function as an endogenous extracellular electron shuttle. This study provides evidence that environmentally triggered changes in secondary metabolite production may provide clues to the ecological functions of specific compounds, and that Gram-positive bacteria considered to be obligate aerobes may play previously unrecognized roles in biogeochemical cycling through mechanisms that include extracellular electron shuttling.

Comparative transcriptomics as a guide to natural product discovery and biosynthetic gene cluster functionality

“…If so, this raises the intriguing possibility that BGCs predicted to encode the biosynthesis of the same compounds may be expressed in response to different environmental cues, and thus serve different ecological functions. While there is evidence that a single biosynthetic pathway yields products with different ecological functions (66), the concept that a single product may serve different functions under different conditions adds considerable complexity to our understanding of chemical ecology (67,68). Alternatively, there may be benefits associated with maintaining certain components of a silent BGC, such as a resistance gene, thereby selecting against loss of the entire cluster.…”

Extending the “One Strain Many Compounds” (OSMAC) Principle to Marine Microorganisms

“…The effect of oxygen concentration on SM production was clearly demonstrated in a recent study conducted on the marine-derived Streptomyces sp. CNQ-525 [ 83 ]. In this study, hypoxia triggered a shift from production of the antibiotic napyradiomycin to production of 8-aminoflaviolin, an intermediate in the napyradiomycin biosynthetic pathway.…”

“…In this study, hypoxia triggered a shift from production of the antibiotic napyradiomycin to production of 8-aminoflaviolin, an intermediate in the napyradiomycin biosynthetic pathway. 8-aminoflaviolin was shown to be a redox active compound, which the authors hypothesized might function as an extracellular electron shuttle [ 83 ]. In batch experiments aeration is often controlled via regulating the shaking speed, and this has also been shown to affect SM production, as for example in the above-mentioned example of TDA production within the Roseobacter clade [ 52 ].…”

The biogeography of Streptomyces in New Zealand enabled by high-throughput sequencing of genus-specific rpoB amplicons

“…Furthermore, their utility as model organisms in investigations of natural product synthesis, cell biology, and evolution has transformed microbiology and biotechnology research (Kämpfer et al, 2014;Chater, 2016). While their capacity for carbon mineralization (Ruddick and Williams, 1972;Barder and Crawford, 1981;Spiker et al, 1992;Dari et al, 1995;Schlatter et al, 2009) and secondary metabolism (Chater, 2016;Niu et al, 2016;Gallagher et al, 2017; have been well-documented, much less is known regarding their diversity, ecology, and biogeography in terrestrial habitats. To date, biogeographical studies of the Streptomyces have largely focused on genetic variation within cultivated representatives to inform population level analyses (Davelos et al, 2004;Antony-Babu et al, 2008;Andam et al, 2016).…”