Abstract

For tolerating extreme desiccation, cyanobacteria are known to produce both compatible solutes at intracellular level and a copious amount of exopolysaccharides as a protective coat. However, these molecules make cyanobacterial cells refractory to a broad spectrum of cell disruption methods, hindering genome sequencing, and molecular studies. In fact, few genomes are already available from cyanobacteria from extremely desiccated environments such as deserts. In this work, we report the 5.4 Mbp draft genome (with 100% of completeness in 105 contigs) of Gloeocapsopsis sp. UTEX B3054 (subsection I; Order Chroococcales), a cultivable sugar-rich and hardly breakable hypolithic cyanobacterium from the Atacama Desert. Our in silico analyses focused on genomic features related to sugar-biosynthesis and adaptation to dryness. Among other findings, screening of Gloeocapsopsis genome revealed a unique genetic potential related to the biosynthesis and regulation of compatible solutes and polysaccharides. For instance, our findings showed for the first time a novel genomic arrangement exclusive of Chroococcaceae cyanobacteria associated with the recycling of trehalose, a compatible solute involved in desiccation tolerance. Additionally, we performed a comparative genome survey and analyses to entirely predict the highly diverse pool of glycosyltransferases enzymes, key players in polysaccharide biosynthesis and the formation of a protective coat to dryness. We expect that this work will set the fundamental genomic framework for further research on microbial tolerance to desiccation and to a wide range of other extreme environmental conditions. The study of microorganisms like Gloeocapsopsis sp. UTEX B3054 will contribute to expand our limited understanding regarding water optimization and molecular mechanisms allowing extremophiles to thrive in xeric environments such as the Atacama Desert.

Highlights

  • The Atacama Desert is the driest warm desert on Earth (Houston and Hartley, 2003; Hartley et al, 2005)

  • UTEX B3054, a unicellular cyanobacterium that we demonstrate belongs to the Chroococcaceae family, and which possesses few known cultivable and sequenced representatives

  • For retrieving a high-quality DNA (260/280 ratio > 1.8) amenable for genome sequencing of the sugar-rich Gloeocapsopsis, it was necessary to massively eliminate heterotrophic bacteria for obtaining a pure and clonal culture, which was performed by single cell sorting coupled to flow cytometry

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Summary

Introduction

The Atacama Desert is the driest warm desert on Earth (Houston and Hartley, 2003; Hartley et al, 2005). Most microbial life in deserts is somehow associated to rocks, developing either within or underneath them (Chan et al, 2012; Pointing and Belnap, 2012; Cowan et al, 2014; Davila et al, 2015; Wierzchos et al, 2015) These microbial communities are dominated by primary producers, represented mainly by morphological and metabolically diverse cyanobacteria (Pointing et al, 2009; Wong et al, 2010; Wierzchos et al, 2015; Wei et al, 2016). Most of these desert cyanobacteria produce copious extracellular structures, a feature that is thought to constitute both the architectural and metabolic basis for the microbial community and its tolerance to extreme environmental conditions (Knowles and Castenholz, 2008; Colica et al, 2014; Rossi and De Philippis, 2015)

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