Abstract
A cultivation-dependent approach revealed that highly diverse populations of Streptomyces were present in atmospheric precipitations from a hailstorm event sampled in February 2016 in the Cantabrian Sea coast, North of Spain. A total of 29 bioactive Streptomyces strains isolated from small samples of hailstone and rainwater, collected from this hailstorm event, were studied here. Taxonomic identification by 16S rRNA sequencing revealed more than 20 different Streptomyces species, with their closest homologs displaying mainly oceanic but also terrestrial origins. Backward trajectory analysis revealed that the air-mass sources of the hailstorm event, with North Western winds, were originated in the Arctic Ocean (West Greenland and North Iceland) and Canada (Labrador), depending on the altitude. After traveling across the North Atlantic Ocean during 4 days the air mass reached Europe and precipitated as hailstone and rain water at the sampling place in Spain. The finding of Streptomyces species able to survive and disperse through the atmosphere increases our knowledge of the biogeography of genus Streptomyces on Earth, and reinforces our previous dispersion model, suggesting a generalized feature for the genus which could have been essential in his evolution. This unique atmospheric-derived Streptomyces collection was screened for production of bioactive secondary metabolites. Analyses of isolates ethyl acetate extracts by LC-UV-MS and further database comparison revealed an extraordinary diversity of bioactive natural products. One hundred molecules were identified, mostly displaying contrasted antibiotic and antitumor/cytotoxic activities, but also antiparasitic, antiviral, anti-inflammatory, neuroprotector, and insecticide properties. More interestingly, 38 molecules not identified in natural products databases might represent new natural products. Our results revealed for the first time an extraordinary diversity of Streptomyces species in the atmosphere able to produce an extraordinary repertoire of bioactive molecules, thus providing a very promising source for the discovery of novel pharmaceutical natural products.
Highlights
Natural products are essential to human health and constitute a primary resource in biomedicine and biotechnology
Streptomyces species have been traditionally considered as soil bacteria, in the last decades became evident their presence and wide distribution in oceanic ecosystems and associated to diverse marine organisms
Previous work in the North Atlantic region, Cantabrian Sea (Bay of Biscay), Northern Spain, revealed the presence of a great number of Streptomyces strains in intertidal seaweeds, and deep-sea coral reef invertebrates at the Aviles Canyon
Summary
Natural products are essential to human health and constitute a primary resource in biomedicine and biotechnology. Streptomyces species (Phylum Actinobacteria) are the most prolific source of bioactive natural products with pharmaceutical activities. Streptomyces species have been traditionally considered as soil bacteria, in the last decades became evident their presence and wide distribution in oceanic ecosystems and associated to diverse marine organisms. Previous work in the North Atlantic region, Cantabrian Sea (Bay of Biscay), Northern Spain, revealed the presence of a great number of Streptomyces strains in intertidal seaweeds, and deep-sea coral reef invertebrates at the Aviles Canyon. New natural products with antimicrobial and cytotoxic activities against tumor cell lines were recently discovered in this submarine Canyon (Braña et al, 2015, 2017a,b; Sarmiento-Vizcaíno et al, 2015, 2016, 2017a,b)
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