Glycerol metabolism in hypersaline environments

Abstract

Summary Glycerol is a key compound for the understanding of the microbiology of hypersaline environments. At the highest salt concentrations the main or even sole primary producer is the green unicellular alga Dunaliella, which uses photosynthetically produced glycerol as osmotic stabilizer and compatible solute. Glycerol can be expected to be a major carbon source available to the heterotrophic communities of Archaea and Bacteria in hypersaline ecosystems. Use of Dunaliella has even been explored for the commercial production of glycerol. This article reviews our current understanding of glycerol metabolism in Dunaliella and of the ways glycerol can be degraded by heterotrophic prokaryote communities under aerobic and under anaerobic conditions. Dunaliella‐derived glycerol may also be the key toward long‐term survival of heterotrophic prokaryotes in fluid inclusions within salt crystals.

A multidomain enzyme, with glycerol‐3‐phosphate dehydrogenase and phosphatase activities, is involved in a chloroplastic pathway for glycerol synthesis in Chlamydomonas reinhardtii

“…Few genes encoding enzymes of glycerol metabolism show altered expression in C. reinhardtii subject to nitrogen deprivation or salinity stress Production of glycerol-3-phosphate and glycerol under nitrogen starvation or hyperosmotic stress likely involves interconversions catalyzed by several enzymes (Wang et al, 2001;Oren, 2017) (Figures 6 and 7). Besides GPD2like chimeric proteins, DHAP conversion to glycerol can be carried out by two canonical enzymes, a standard GPD (like GPD1 or GPD5) and a glycerol-3-phosphate phosphatase (GPP) (Figure 7).…”

“…Conversely, glycerol can be converted to G3P by a glycerol kinase (GK) and to DHAP by a glycerol 2-dehydrogenase and a dihydroxyacetone kinase (DAK) ( Figure 7). In Dunaliella, several of these enzymes were proposed to constitute a glycerol cycle, involving specific pathways for glycerol synthesis and for glycerol removal during the osmoregulatory process (Ben-Amotz et al, 1982;Chen et al, 2012;Oren, 2017). Putative orthologs of these enzymes encoded in the C. reinhardtii genome were identified by homology searches, and their roles are indicated in Figure 7 (yellow box).…”

“…As already mentioned, G3P is the precursor for the backbone of glycerolipids, with TAGs accumulating as carbon and energy reserves under nutrient deprivation (Hu et al, 2008;Radakovits et al, 2010;Msanne et al, 2012;Johnson and Alric, 2013;Morales-S anchez et al, 2013;Zienkiewicz et al, 2016). Conversely, glycerol is involved in algal acclimation to high salinity as osmotic stabilizer and compatible solute that allows maintenance of enzyme activities under conditions of low water activity (Ben-Amotz and Avron, 1973;Ben-Amotz et al, 1982;Goshal et al, 2002;Goyal, 2007;Chen and Jiang, 2009;Chen et al, 2011;Oren, 2017). Figure 7.…”

“…Indeed, GPDs are commonly involved in glycerolipid metabolism and in the preservation of cellular redox status by consuming NAD(P)H and regenerating NAD(P) + (Kl€ ock and Kreuzberg, 1989;Wang et al, 2001;Goshal et al, 2002). These enzymes have also been implicated in osmotic stress acclimation in several algal species of the genera Dunaliella, Asteromonas and Chlamydomonas (Ben-Amotz et al, 1982;Kl€ ock and Kreuzberg, 1989;Gee et al, 1993;Goshal et al, 2002;Oren, 2017). GPDs play a role in the response to osmotic and salinity stress by affecting the synthesis of glycerol, a known osmoprotectant (Ben-Amotz et al, 1982;Goshal et al, 2002).…”

Prospects for harnessing biocide resistance for bioremediation and detoxification

“…Oil spills in arid terrestrial environments are accompanied by the simultaneous occurrence of high pH, high salinity, and high loads of toxic organic compounds. In general, adaptation to osmotic stress under high salinity and pH requires increased intracellular salt concentration or accumulation of organic osmotic solutes (30). At elevated salinity, the microbial cell surface tends to become more hydrophilic, which will further limit physiological activity on hydrophobic hydrocarbons.…”