Actinobacterial Rare Biospheres and Dark Matter Revealed in Habitats of the Chilean Atacama Desert

Abstract

The Atacama Desert is the most extreme non-polar biome on Earth, the core region of which is considered to represent the dry limit for life and to be an analogue for Martian soils. This study focused on actinobacteria because they are keystone species in terrestrial ecosystems and are acknowledged as an unrivalled source of bioactive compounds. Metagenomic analyses of hyper-arid and extreme hyper-arid soils in this desert revealed a remarkable degree of actinobacterial ‘dark matter’, evidenced by a detected increase of 34% in families against those that are validly published. Rank-abundance analyses indicated that these soils were high-diversity habitats and that the great majority of designated ‘rare’ genera (up to 60% of all phylotypes) were always rare. These studies have enabled a core actinobacterial microbiome common to both habitats to be defined. The great majority of detected taxa have not been recovered by culture dependent methods, neither, with very few exceptions, has their functional ecology been explored. A microbial seed bank of this magnitude has significance not just for Atacama soil ecosystem resilience but represents an enormous untapped resource for biotechnology discovery programmes in an era where resistance to existing antibiotics is rapidly becoming a major threat to global health.

Extreme environments: microbiology leading to specialized metabolites

“…Actinobacteria that are amycelial or form rudimentary hyphae have received less attention though they are known to be common in desert soils (Idris et al 2017b;Bull et al 2018b). Members of the family Geodermatophilaceae have received the most attention, notably the genera Blastococcus, Geodermatophilus and Modestobacter; members of these taxa are known to be resistant to desiccation, ionizing radiation, UV-light and heavy metals (Sghaier et al 2016 (Thumar et al 2010).…”

Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 m of bioprospecting campaigns

“…Culture-based surveys of recent years have reported members of over 23 validly named genera and many new and putatively new species have been highlighted including ones belonging to the poorly studied genera Actinomadura, Cryptosporangium, Kribbela, Nonomuraea, Pseudonocardia and Saccharothrix [26,27]. However, it is only from the results of metagenomic surveys that the spectacular extent of actinobacterial diversity in Atacama habitats has been fully recognised [28,29]. The data in Table 2 show the massive extent of actinobacterial dark matter existing at suprageneric ranks while at the genus rank 234 and 297 phylotypes were detected at low and high altitude sites, respectively.…”

“…Genomes of members of the family Geodermatophilaceae isolated from extreme hyper-arid soils were relatively small (3.89-5.51 Mb) but contained a high proportion of genes related to environmental stress response including heat and cold shock responses, osmotic stress, carbon starvation and stress factors that give rise to reactive oxygen species [28,29,49]. Perhaps surprising is the high capacity of these bacteria to synthesis specialized metabolites, a feature also noted in novel species of Micromonospora isolated from extreme hyper-arid Lomas Bayas soil [52], the assumption being that competitive success in extreme, sparsely populated ecosystems might be more likely determined by stress resistance rather than by antibiosis.…”

Modestobacter altitudinis sp. nov., a novel actinobacterium isolated from Atacama Desert soil

“…excelsi' [3]. These results go someway towards accounting for the high numbers of Geodermatophilaceae propagules present in Atacama Desert habitats where extreme environmental conditions prevail [11,19]. Indeed, these data lend support to the view that the competitive success of these organisms in extreme, sparsely populated biomes may be a function of stress resistance not antibiosis [12].…”

“…Continued [4,8], Modestobacter marinus from deep-sea sediment [9] and Modestobacter caceresii and 'Modestobacter excelsi' from hyper-arid Atacama Desert soils [3,10]. Culture-independent studies show that Modestobacter strains are key components of Atacama Desert soils [11,12] characterised by scarcity of liquid water, low concentrations of organic carbon and high solar irradiation [13][14][15]. In light of such considerations it is interesting that the genomes of the type strains of M. caceresii and 'M.…”