An extremely halophilic proteobacterium combines a highly acidic proteome with a low cytoplasmic potassium content

Ratnakar Deole, Jean Challacombe, Douglas W. Raiford, Wouter D. Hoff

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

Halophilic archaea accumulate molar concentrations of KCl in their cytoplasm as an osmoprotectant and have evolved highly acidic proteomes that function only at high salinity. We examined osmoprotection in the photosynthetic Proteobacteria Halorhodospira halophila and Halorhodospira halochloris. Genome sequencing and isoelectric focusing gel electrophoresis showed that the proteome of H. halophila is acidic. In line with this finding, H. halophila accumulated molar concentrations of KCl when grown in high salt medium as detected by x-ray micro-analysis and plasma emission spectrometry. This result extends the taxonomic range of organisms using KCl as a main osmoprotectant to the Proteobacteria. The closely related organism H. halochloris does not exhibit an acidic proteome, matching its inability to accumulate K+. This observation indicates recent evolutionary changes in the osmoprotection strategy of these organisms. Upon growth of H. halophila in low salt medium, its cytoplasmic K+ content matches that of Escherichia coli, revealing an acidic proteome that can function in the absence of high cytoplasmic salt concentrations. These findings necessitate a reassessment of two central aspects of theories for understanding extreme halophiles. First, we conclude that proteome acidity is not driven by stabilizing interactions between K+ ions and acidic side chains but by the need for maintaining sufficient solvation and hydration of the protein surface at high salinity through strongly hydrated carboxylates. Second, we propose that obligate protein halophilicity is a non-adaptive property resulting from genetic drift in which constructive neutral evolution progressively incorporates weakly stabilizing K +-binding sites on an increasingly acidic protein surface.

Original languageEnglish
Pages (from-to)581-588
Number of pages8
JournalJournal of Biological Chemistry
Volume288
Issue number1
DOIs
StatePublished - 4 Jan 2013
Externally publishedYes

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Halorhodospira halophila
Proteobacteria
Proteome
Potassium
Genetic Drift
Salts
Salinity
Halobacteriales
Membrane Proteins
Archaea
Solvation
Isoelectric Focusing
Electrophoresis
Acidity
Hydration
Escherichia coli
Spectrometry
Spectrum Analysis
Cytoplasm
Genes

Cite this

Deole, Ratnakar ; Challacombe, Jean ; Raiford, Douglas W. ; Hoff, Wouter D. / An extremely halophilic proteobacterium combines a highly acidic proteome with a low cytoplasmic potassium content. In: Journal of Biological Chemistry. 2013 ; Vol. 288, No. 1. pp. 581-588.
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An extremely halophilic proteobacterium combines a highly acidic proteome with a low cytoplasmic potassium content. / Deole, Ratnakar; Challacombe, Jean; Raiford, Douglas W.; Hoff, Wouter D.

In: Journal of Biological Chemistry, Vol. 288, No. 1, 04.01.2013, p. 581-588.

Research output: Contribution to journalArticle

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