Trehalose/2-sulfotrehalose biosynthesis and glycine-betaine uptake are widely spread mechanisms for osmoadaptation in the Halobacteriales

Abstract

We investigated the mechanisms of osmoadaptation in the order Halobacteriales, with special emphasis on Haladaptatus paucihalophilus, known for its ability to survive in low salinities. H. paucihalophilus genome contained genes for trehalose synthesis (trehalose-6-phosphate synthase/trehalose-6-phosphatase (OtsAB pathway) and trehalose glycosyl-transferring synthase pathway), as well as for glycine betaine uptake (BCCT family of secondary transporters and QAT family of ABC transporters). H. paucihalophilus cells synthesized and accumulated B1.97-3.72 lmol per mg protein of trehalose in a defined medium, with its levels decreasing with increasing salinities. When exogenously supplied, glycine betaine accumulated intracellularly with its levels increasing at higher salinities. RT-PCR analysis strongly suggested that H. paucihalophilus utilizes the OtsAB pathway for trehalose synthesis. Out of 83 Halobacteriales genomes publicly available, genes encoding the OtsAB pathway and glycine betaine BCCT family transporters were identified in 38 and 60 genomes, respectively. Trehalose (or its sulfonated derivative) production and glycine betaine uptake, or lack thereof, were experimentally verified in 17 different Halobacteriales species. Phylogenetic analysis suggested that trehalose synthesis is an ancestral trait within the Halobacteriales, with its absence in specific lineages reflecting the occurrence of gene loss events during Halobacteriales evolution. Analysis of multiple culture-independent survey data sets demonstrated the preference of trehalose-producing genera to saline and low salinity habitats, and the dominance of genera lacking trehalose production capabilities in permanently hypersaline habitats. This study demonstrates that, contrary to current assumptions, compatible solutes production and uptake represent a common mechanism of osmoadaptation within the Halobacteriales.

Patterns and Determinants of Halophilic Archaea (Class Halobacteria) Diversity in Tunisian Endorheic Salt Lakes and Sebkhet Systems

“…Our previous study (37) has provided experimental and genomic evidence that multiple Halobacteria genera are capable of trehalose or 2-sulfotrehalose biosynthesis as an osmoadaptive strategy and that the otsAB operon (encoding trehalose-6-phosphate synthase/trehalose-6-phosphatase) mediates trehalose biosynthesis in the Halobacteria. Further, analysis of the occurrence patterns of otsAB genes demonstrates a distinct phylogenetic pattern, where the otsAB operon was identified in all members of Halobacteria clade I (as defined in references 42 and 43), as well as in the genera Halococcus, Haladaptatus, Halalkalicoccus, and Halosimplex.…”

“…In addition to salting in, some members of the Halobacteria maintain high intracellular osmotic pressure by synthesis and/or uptake of highly soluble organic solutes that do not interfere with intracellular enzymatic activities and cellular processes. We have recently demonstrated that multiple genera within the Halobacteria biosynthesize and accumulate molar levels of trehalose (or 2-sulfotrehalose) as an osmoadaptive compatible solute (37). Currently, the impact of the possession (or lack thereof) of such a capability within members of the Halobacteria on their ecological fitness, habitat preferences, and, consequently, the overall Halobacteria community structure within a specific saline or hypersaline habitat is unclear.…”

“…The most prevalent mechanism for osmoadaptation is "salting in," where cells accumulate molar concentrations of potassium ions to counter the high extracellular osmotic pressure. This strategy appears to be universally adapted by all members of the Halobacteria (37,38). In addition to salting in, some members of the Halobacteria maintain high intracellular osmotic pressure by synthesis and/or uptake of highly soluble organic solutes that do not interfere with intracellular enzymatic activities and cellular processes.…”

Dynamic Metabolic and Transcriptional Profiling of Rhodococcus sp. Strain YYL during the Degradation of Tetrahydrofuran

“…It is interesting to notice the different alterations of TMAO from trehalose as well, for which a reasonable explanation could be that strain YYL has multiple compatible solute systems in response to different stresses. The presence of different osmoadaptation mechanisms was also found in the Halobacteriales (55). A bacterium could also asymmetrically respond to different stresses (56).…”

Extremophile Current Challenges and New Gate of Knowledge by Nanoparticles Pathways.

“…Compatible solution including proline, glutamate, carnitine, betaine, glycine, ectoine, and exotic compatible solutes as 2-sulfotrehalose [51,52].In environmental isotonic,the accumulation of salts like KCl or NaCl are in equal concentrations. As a results, the concentration of high salts have been copied by halophilic proteins (e.g.…”