Unveiling metabolic pathways involved in the extreme desiccation tolerance of an Atacama cyanobacterium

Abstract

Gloeocapsopsis dulcis strain AAB1 is an extremely xerotolerant cyanobacterium isolated from the Atacama Desert (i.e., the driest and oldest desert on Earth) that holds astrobiological significance due to its ability to biosynthesize compatible solutes at ultra-low water activities. We sequenced and assembled the G. dulcis genome de novo using a combination of long- and short-read sequencing, which resulted in high-quality consensus sequences of the chromosome and two plasmids. We leveraged the G. dulcis genome to generate a genome-scale metabolic model (iGd895) to simulate growth in silico. iGd895 represents, to our knowledge, the first genome-scale metabolic reconstruction developed for an extremely xerotolerant cyanobacterium. The model's predictive capability was assessed by comparing the in silico growth rate with in vitro growth rates of G. dulcis, in addition to the synthesis of trehalose. iGd895 allowed us to explore simulations of key metabolic processes such as essential pathways for water-stress tolerance, and significant alterations to reaction flux distribution and metabolic network reorganization resulting from water limitation. Our study provides insights into the potential metabolic strategies employed by G. dulcis, emphasizing the crucial roles of compatible solutes, metabolic water, energy conservation, and the precise regulation of reaction rates in their adaptation to water stress.