A potassium chloride to glycine betaine osmoprotectant switch in the extreme halophile Halorhodospira halophila

Ratnakar Deole,Wouter D Hoff

doi:10.1038/s41598-020-59231-9

Abstract

Halophiles utilize two distinct osmoprotection strategies. The accumulation of organic compatible solutes such as glycine betaine does not perturb the functioning of cytoplasmic components, but represents a large investment of energy and carbon. KCl is an energetically attractive alternative osmoprotectant, but requires genome-wide modifications to establish a highly acidic proteome. Most extreme halophiles are optimized for the use of one of these two strategies. Here we examine the extremely halophilic Proteobacterium Halorhodospira halophila and report that medium K+ concentration dramatically alters its osmoprotectant use. When grown in hypersaline media containing substantial K+ concentrations, H. halophila accumulates molar concentrations of KCl. However, at limiting K+ concentrations the organism switches to glycine betaine as its major osmoprotectant. In contrast, the closely related organism Halorhodospira halochloris is limited to using compatible solutes. H. halophila performs both de novo synthesis and uptake of glycine betaine, matching the biosynthesis and transport systems encoded in its genome. The medium K+ concentration (~10 mM) at which the KCl to glycine betaine osmoprotectant switch in H. halophila occurs is near the K+ content of the lake from which it was isolated, supporting an ecological relevance of this osmoprotectant strategy.

Highlights

All halophilic organisms face the risk of cellular dehydration caused by the high osmotic activity of saline environments, and require osmoprotection strategies to survive
Halophilic microorganisms manage to thrive in saline and even hypersaline environments by increasing the osmotic activity of their cytoplasm to match that of the environment
While H. halochloris has been shown to utilize glycine betaine as its main osmoprotectant[34], we found that H. halophila predominantly accumulates molar concentrations of KCl28

Summary

Introduction

All halophilic organisms face the risk of cellular dehydration caused by the high osmotic activity of saline environments, and require osmoprotection strategies to survive. Two types of osmoadaptive strategies are employed by halophiles and extreme halophiles[4,5,6,7]: either the accumulation of molar concentrations of KCl or the accumulation of organic compounds such as glycine betaine compatible solutes in their cytoplasm[8,9,10,11] Which of these two main osmoprotection strategies an organism utilizes has profound implications for its ecology, physiology, biochemistry, and evolutionary history. While H. halochloris has been shown to utilize glycine betaine as its main osmoprotectant[34], we found that H. halophila predominantly accumulates molar concentrations of KCl28 This result implies a relatively recent and dramatic evolutionary change in osmoprotection strategy. While most extreme halophiles are believed to dedicate their osmoprotection strategy either to the use of KCl or organic osmoprotectants, here we report the existence of an “omoprotection switch” in H. halophila, allowing this organism to switch between the KCl and organic osmoprotectant strategies depending on environmental conditions

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