Actinobacterial diversity in Atacama Desert habitats as a road map to biodiscovery

Abstract

The Atacama Desert of Northern Chile, the oldest and driest nonpolar desert on the planet, is known to harbour previously undiscovered actinobacterial taxa with the capacity to synthesize novel natural products. In the present study, culture-dependent and culture-independent methods were used to further our understanding of the extent of actinobacterial diversity in Atacama Desert habitats. The culture-dependent studies focused on the selective isolation, screening and dereplication of actinobacteria from high altitude soils from Cerro Chajnantor. Several strains, notably isolates designated H9 and H45, were found to produce new specialized metabolites. Isolate H45 synthesized six novel metabolites, lentzeosides A-F, some of which inhibited HIV-1 integrase activity. Polyphasic taxonomic studies on isolates H45 and H9 showed that they represented new species of the genera Lentzea and Streptomyces, respectively; it is proposed that these strains be designated as Lentzea chajnantorensis sp. nov. and Streptomyces aridus sp. nov.. Additional isolates from sampling sites on Cerro Chajnantor were considered to be nuclei of novel species of Actinomadura, Amycolatopsis, Cryptosporangium and Pseudonocardia. A majority of the isolates produced bioactive compounds that inhibited the growth of one or more strains from a panel of six wild type microorganisms while those screened against Bacillus subtilis reporter strains inhibited sporulation and cell envelope, cell wall, DNA and fatty acid synthesis. Initial culture-independent studies were carried out to establish the extent of actinobacterial diversity in a range of hyper- and extreme hyper-arid Atacama Desert soils. Community DNA extracted from soil collected from the sampling sites was surveyed for actinobacteria by 454 pyrosequencing; rarefaction analyses indicated good coverage at most of the sites. The results revealed an amazing and unexpected taxonomic diversity at the ranks of order, family and genus, much of it novel. The total number of genera, for instance, is 328, of which around 40% could not be assigned to validly published genera. Rank abundancy profiles indicated that much of this diversity can be attributed to low abundancy taxa. Similar results were obtained from community DNA extracted from surface and subsurface soil samples collected at three different altitudes on Cerro Chajnantor. Actinobacterial community structure at these sampling sites was influenced by altitude and sampling depth, as well as several environmental variables that included conductivity, pH, redox potential and organic matter content. It is evident from these studies that the Atacama Desert landscape abounds in novel actinobacterial taxa that synthesize a broad range of specialized metabolites that can be developed as drug leads.