Calculation of the Relative Chemical Stabilities of Proteins as a Function of Temperature and Redox Chemistry in a Hot Spring

Jeffrey M Dick,Everett L Shock,Jonathan H Badger

doi:10.1371/journal.pone.0022782

Abstract

Uncovering the chemical and physical links between natural environments and microbial communities is becoming increasingly amenable owing to geochemical observations and metagenomic sequencing. At the hot spring known as Bison Pool in Yellowstone National Park, the cooling of the water in the outflow channel is associated with an increase in oxidation potential estimated from multiple field-based measurements. Representative groups of proteins whose sequences were derived from metagenomic data also exhibit an increase in average oxidation state of carbon in the protein molecules with distance from the hot-spring source. The energetic requirements of reactions to form selected proteins used in the model were computed using amino-acid group additivity for the standard molal thermodynamic properties of the proteins, and the relative chemical stabilities of the proteins were investigated by varying temperature, pH and oxidation state, expressed as activity of dissolved hydrogen. The relative stabilities of the proteins were found to track the locations of the sampling sites when the calculations included a function for hydrogen activity that increases with temperature and is higher, or more reducing, than values consistent with measurements of dissolved oxygen, sulfide and oxidation-reduction potential in the field. These findings imply that spatial patterns in the amino acid compositions of proteins can be linked, through energetics of overall chemical reactions representing the formation of the proteins, to the environmental conditions at this hot spring, even if microbial cells maintain considerably different internal conditions. Further applications of the thermodynamic calculations are possible for other natural microbial ecosystems.

Highlights

The imprints of distinct geochemical environments can be found in the molecular compositions of microbial genomes and their protein products
It can be shown that the Gibbs energy change in overall chemical reactions to synthesize amino acids from from inorganic species depends on environmental conditions [9]
Description of field site and metagenomic sampling Chemical and biological sampling was performed in July 2005 at the hot spring known as ‘‘Bison Pool’’ in the Sentinel Meadows in the Lower Geyser Basin of Yellowstone National Park [12]. ‘‘Bison Pool’’ is the unofficial name of a hot spring whose source pool is located at approximately 44.56961uN, 110.86513uW (WGS 84 datum), the closest officially named feature being called Rosette Geyser [49]

Summary

Introduction

The imprints of distinct geochemical environments can be found in the molecular compositions of microbial genomes and their protein products. The biosynthetic costs of amino acids have been estimated from metabolic constraints including numbers of phosphate bonds and hydrogen atoms transferred during synthesis from precursors [6,8]. Those estimates depend on the growth medium and specific metabolic pathways but otherwise do not involve environmental variables such as temperature and oxidation-reduction conditions. It can be shown that the Gibbs energy change in overall chemical reactions to synthesize amino acids from from inorganic species depends on environmental conditions [9]. The calculations of energetics of overall synthesis reactions can be done for proteins, where group additivity methods permit assessing standard Gibbs energies of proteins of any amino acid composition [10,11]

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