The halophilic alkalithermophile Natranaerobius thermophilus adapts to multiple environmental extremes using a large repertoire of Na(K)/H antiporters.

Noha M Mesbah,Gregory M Cook,Juergen Wiegel

doi:10.1111/j.1365-2958.2009.06845.x

Noha M Mesbah, Gregory M Cook + Show 1 more

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https://doi.org/10.1111/j.1365-2958.2009.06845.x

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Abstract

Natranaerobius thermophilus is an unusual extremophile because it is halophilic, alkaliphilic and thermophilic, growing optimally at 3.5 M Na+, pH55°C 9.5 and 53°C. Mechanisms enabling this tripartite lifestyle are essential for understanding how microorganisms grow under inhospitable conditions, but remain unknown, particularly in extremophiles growing under multiple extremes. We report on the response of N. thermophilus to external pH at high salt and elevated temperature and identify mechanisms responsible for this adaptation. N. thermophilus exhibited cytoplasm acidification, maintaining an unanticipated transmembrane pH gradient of 1 unit over the entire extracellular pH range for growth. N. thermophilus uses two distinct mechanisms for cytoplasm acidification. At extracellular pH values at and below the optimum, N. thermophilus utilizes at least eight electrogenic Na+(K+)/H+ antiporters for cytoplasm acidification. Characterization of these antiporters in antiporter-deficient Escherichia coli KNabc showed overlapping pH profiles (pH 7.8–10.0) and Na+ concentrations for activity (K0.5 values 1.0–4.4 mM), properties that correlate with intracellular conditions of N. thermophilus. As the extracellular pH increases beyond the optimum, electrogenic antiport activity ceases, and cytoplasm acidification is achieved by energy-independent physiochemical effects (cytoplasmic buffering) potentially mediated by an acidic proteome. The combination of these strategies allows N. thermophilus to grow over a range of extracellular pH and Na+ concentrations and protect biomolecules under multiple extreme conditions.

Highlights

Extremophilic microorganisms are excellent models for the study and characterization of novel physiologies and biochemical pathways, and are models for possible extraterrestrial life
See Wiegel (1998) for more details]. These microorganisms are thermophilic, alkaliphilic and halophilic, and these growth conditions place them into the unusual group of ‘poly extremophiles’, termed the halophilic alkalithermophiles
The obligately anaerobic N. thermophilus is able to grow in the pH55°C range 8.3–10.6 and no growth is observed below pH55°C 8.2 and above pH55°C 10.8 (Fig. 1A)

Summary

Introduction

Extremophilic microorganisms are excellent models for the study and characterization of novel physiologies and biochemical pathways, and are models for possible extraterrestrial life. Recent work from our laboratory has described the isolation and characterization of novel anaerobic bacteria growing at a unique combination of extreme conditions (Mesbah et al, 2007; Mesbah and Wiegel, 2009). The taxa of halophilic alkalithermophiles isolated far represent a novel order within the Firmicutes, the Natranaerobiales (Mesbah et al, 2007; Mesbah and Wiegel, 2009) Their high pH and temperature optima/maxima for growth distinguish them from other anaerobic halophiles within the Firmicutes

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Conclusion