Abstract
Members of the genus Spiribacter are found worldwide and are abundant in ecosystems possessing intermediate salinities between seawater and saturated salt concentrations. Spiribacter salinus M19-40 is the type species of this genus and its first cultivated representative. In the habitats of S. salinus M19-40, high salinity is a key determinant for growth and we therefore focused on the cellular adjustment strategy to this persistent environmental challenge. We coupled these experimental studies to the in silico mining of the genome sequence of this moderate halophile with respect to systems allowing this bacterium to control its potassium and sodium pools, and its ability to import and synthesize compatible solutes. S. salinus M19-40 produces enhanced levels of the compatible solute ectoine, both under optimal and growth-challenging salt concentrations, but the genes encoding the corresponding biosynthetic enzymes are not organized in a canonical ectABC operon. Instead, they are scrambled (ectAC; ectB) and are physically separated from each other on the S. salinus M19-40 genome. Genomes of many phylogenetically related bacteria also exhibit a non-canonical organization of the ect genes. S. salinus M19-40 also synthesizes trehalose, but this compatible solute seems to make only a minor contribution to the cytoplasmic solute pool under osmotic stress conditions. However, its cellular levels increase substantially in stationary phase cells grown under optimal salt concentrations. In silico genome mining revealed that S. salinus M19-40 possesses different types of uptake systems for compatible solutes. Among the set of compatible solutes tested in an osmostress protection growth assay, glycine betaine and arsenobetaine were the most effective. Transport studies with radiolabeled glycine betaine showed that S. salinus M19-40 increases the pool size of this osmolyte in a fashion that is sensitively tied to the prevalent salinity of the growth medium. It was amassed in salt-stressed cells in unmodified form and suppressed the synthesis of ectoine. In conclusion, the data presented here allow us to derive a genome-scale picture of the cellular adjustment strategy of a species that represents an environmentally abundant group of ecophysiologically important halophilic microorganisms.
Highlights
The earth possesses widely distributed hypersaline ecosystems in which the main life-limiting factor is their high salt concentration (Ventosa et al, 1998; Grant, 2004)
To assess the amount of NaCl needed for its growth and the ability of S. salinus M19-40 to colonize hypersaline habitats, cells were propagated in SMM with increasing concentrations of NaCl
S. salinus M19-40 depends on a considerable salt concentration for its growth but it can cope with a broad spectrum of salinities
Summary
The earth possesses widely distributed hypersaline ecosystems in which the main life-limiting factor is their high salt concentration (Ventosa et al, 1998; Grant, 2004). Most microbiological studies of these extreme ecosystems have been carried out on aquatic habitats, such as saline lakes and marine salterns. Salterns constitute excellent models for the study of the diversity and ecology of microorganisms that either strive or struggle under high-saline growth conditions (Ventosa et al, 2014, 2015). The isolation of the most abundant types of microorganisms from hypersaline habitats is challenging (Ventosa et al, 2014), because their cultivation for laboratory studies is difficult and tedious. The physiology of these microorganisms is typically assessed indirectly through metagenomic approaches (Ventosa et al, 2015), or, at best, studied in a few isolated species serving as proxy (Grote et al, 2012; Swan et al, 2013; Carini et al, 2014; Suh et al, 2015)
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