Abstract
An extreme halophilic archaeon, strain SGH1, is a novel microorganism isolated from endolithic microbial communities colonizing halites at Salar Grande, Atacama Desert, in northern Chile. Our study provides structural, biochemical, genomic, and physiological information on this new isolate living at the edge of the physical and chemical extremes at the Atacama Desert. SGH1 is a Gram-negative, red-pigmented, non-motile unicellular coccoid organism. Under the transmission electron microscope, strain SGH1 showed an abundant electro-dense material surrounding electron-lucent globular structures resembling gas vacuoles. Strain SGH1 showed a 16S rRNA gene sequence with a close phylogenetic relationship to the extreme halophilic archaea Haloterrigena turkmenica and Haloterrigena salina and has been denominated Haloterrigena sp. strain SGH1. Strain SGH1 grew at 20–40°C (optimum 37°C), at salinities between 15 and 30% (w/v) NaCl (optimum 25%) and growth was improved by addition of 50 mM KCl and 0.5% w/v casamino acids. Growth was severely restricted at salinities below 15% NaCl and cell lysis is avoided at a minimal 10% NaCl. Maximal concentrations of magnesium chloride and sodium or magnesium perchlorates that supported SGH1 growth were 0.5 and 0.15M, respectively. Haloterrigena sp. strain SGH1 accumulates bacterioruberin (BR), a C50 xanthophyll, as the major carotenoid. Total carotenoids in strain SGH1 amounted to nearly 400 μg BR per gram of dry biomass. Nearly 80% of total carotenoids accumulated as geometric isomers of BR: all-trans-BR (50%), 5-cis-BR (15%), 9-cis-BR (10%), 13-cis-BR (4%); other carotenoids were dehydrated derivatives of BR. Carotenogenesis in SGH1 was a reversible and salt-dependent process; transferring BR-rich cells grown in 25% (w/v) NaCl to 15% (w/v) NaCl medium resulted in depigmentation, and BR content was recovered after transference and growth of unpigmented cells to high salinity medium. Methanol extracts and purified BR isomers showed an 8–9-fold higher antioxidant activity than Trolox or β-carotene. Both, plasma membrane integrity and mitochondrial membrane potential measurements under acute 18-h assays showed that purified BR isomers were non-toxic to cultured human THP-1 cells.
Highlights
The Atacama Desert is considered to be the driest and oldest dryland on Earth (McKay et al, 2003; Navarro-González et al, 2003)
We provide structural and biochemical information on strain SGH1 and on the identification, content, antioxidant properties and toxicity of its BR isomers
Strain SGH1 only occurred as one type of a Gramnegative, non-motile coccoid microorganism with an average diameter of 1–2 μm
Summary
The Atacama Desert is considered to be the driest and oldest dryland on Earth (McKay et al, 2003; Navarro-González et al, 2003). Lithobiontic colonization can be considered as one of the most successful strategies for microbial survival under the extreme desiccation and high solar radiation on the Atacama Desert. Lithic habitats provide one of the most efficient niches to sustain microbial life by acting as a filter to solar and ultraviolet radiations, as a liquid water harvesting device from fogs and dew events, by salt deliquescence and capillary condensation (Davila et al, 2008; Wierzchos et al, 2015, 2018; Cockell et al, 2017; Gómez-Silva, 2018; Meslier et al, 2018; Uritskiy et al, 2019). In Atacama, lithic habitats such as halite nodules are colonized by endolithic and epilithic microbial consortia that include members of the three domains of life and viruses (de los Ríos et al, 2010; Gómez-Silva, 2010, 2018; Robinson et al, 2015; Crits-Christoph et al, 2016a,b; Wierzchos et al, 2018)
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