Abstract
Actinobacteria are the main producers of bioactive natural products essential for human health. Although their diversity in the atmosphere remains largely unexplored, using a multidisciplinary approach, we studied here 27 antibiotic producing Actinobacteria strains, isolated from 13 different precipitation events at three locations in Northern and Southern Spain. Rain samples were collected throughout 2013–2016, from events with prevailing Western winds. NOAA HYSPLIT meteorological analyses were used to estimate the sources and trajectories of the air-mass that caused the rainfall events. Five-day backward air masses trajectories of the diverse events reveals a main oceanic source from the North Atlantic Ocean, and in some events long range transport from the Pacific and the Arctic Oceans; terrestrial sources from continental North America and Western Europe were also estimated. Different strains were isolated depending on the precipitation event and the latitude of the sampling site. Taxonomic identification by 16S rRNA sequencing and phylogenetic analysis revealed these strains to belong to two Actinobacteria genera. Most of the isolates belong to the genus Streptomyces, thus increasing the number of species of this genus isolated from the atmosphere. Furthermore, five strains belonging to the rare Actinobacterial genus Nocardiopsis were isolated in some events. These results reinforce our previous Streptomyces atmospheric dispersion model, which we extend herein to the genus Nocardiopsis. Production of bioactive secondary metabolites was analyzed by LC-UV-MS. Comparative analyses of Streptomyces and Nocardiopsis metabolites with natural product databases led to the identification of multiple, chemically diverse, compounds. Among bioactive natural products identified 55% are antibiotics, both antibacterial and antifungal, and 23% have antitumor or cytotoxic properties; also compounds with antiparasitic, anti-inflammatory, immunosuppressive, antiviral, insecticidal, neuroprotective, anti-arthritic activities were found. Our findings suggest that over time, through samples collected from different precipitation events, and space, in different sampling places, we can have access to a great diversity of Actinobacteria producing an extraordinary reservoir of bioactive natural products, from remote and very distant origins, thus highlighting the atmosphere as a contrasted source for the discovery of novel compounds of relevance in medicine and biotechnology.
Highlights
In nature, members of the Phylum Actinobacteria continue to be the main producers of structurally diverse bioactive natural products, essential for human health
In a culture dependent approach, we provide here further insights into the phylogenetic and secondary metabolic diversity of bioactive atmospheric Actinobacteria isolated from rainwater
From a total of 169 compounds detected after LC/MS dereplication, 82.25% were identified in the Dictionary of Natural Products, whereas, remarkably, the remaining 17.75%, not found in DPN, might be new molecules and deserve further research
Summary
Members of the Phylum Actinobacteria continue to be the main producers of structurally diverse bioactive natural products, essential for human health. Previous reports in oceanic and atmospheric environments of the Cantabrian Sea region (North Spain, Northeast Atlantic) revealed that phylogenetically diverse Actinobacteria, with a great pharmacological potential, are widespread among intertidal and subtidal seaweeds (Braña et al, 2015; Sarmiento-Vizcaíno et al, 2016) and among deepsea coral reefs ecosystems (Sarmiento-Vizcaíno et al, 2017b), where a novel barotolerant actinobacterium, Myceligenerans cantabricum, was isolated (Sarmiento-Vizcaíno et al, 2015) Some of these marine strains were the source of nine new biologically active natural products with antibiotic properties against clinically relevant antibiotic resistant pathogens and cytotoxic activities toward diverse human cancer cell lines (Braña et al, 2017a,b; Sarmiento-Vizcaíno et al, 2017b; Ortiz-López et al, 2018; Rodríguez et al, 2018)
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