Uncovering chemical signatures of salinity gradients through compositional analysis of protein sequences

Abstract

Abstract. Prediction of the direction of change of a system under specified environmental conditions is one reason for the widespread utility of thermodynamic models in geochemistry. However, thermodynamic influences on the chemical compositions of proteins in nature have remained enigmatic despite much work that demonstrates the impact of environmental conditions on amino acid frequencies. Here, we present evidence that the dehydrating effect of salinity is detectable as chemical differences in protein sequences inferred from (1) metagenomes and metatranscriptomes in regional salinity gradients and (2) differential gene and protein expression in microbial cells under hyperosmotic stress. The stoichiometric hydration state (nH2O), derived from the number of water molecules in theoretical reactions to form proteins from a particular set of basis species (glutamine, glutamic acid, cysteine, O2, H2O), decreases along salinity gradients, including the Baltic Sea and Amazon River and ocean plume, and decreases in particle-associated compared to free-living fractions. However, the proposed metric does not respond as expected for hypersaline environments. Analysis of data compiled for hyperosmotic stress experiments under controlled laboratory conditions shows that differentially expressed proteins are on average shifted toward lower nH2O. Notably, the dehydration effect is stronger for most organic solutes compared to NaCl. This new method of compositional analysis can be used to identify possible thermodynamic effects in the distribution of proteins along chemical gradients at a range of scales from microbial mats to oceans.