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.
Highlights
How microbial populations adapt to environmental gradients is a major challenge at the intersection of geochemistry, microbiology, and biochemistry
Through the compositional analysis of representative metagenomic and metatranscriptomic datasets, we show that ZC and nH2O are most closely aligned with environmental redox and salinity gradients, respectively
The theoretical novelty of this study is the derivation of a compositional metric for stoichiometric hydration state that is largely decoupled from changes in oxidation state (ZC) of proteins
Summary
How microbial populations adapt to environmental gradients is a major challenge at the intersection of geochemistry, microbiology, and biochemistry. Patterns of amino acid usage in proteins are important indicators of microbial adaptation, and amino acid composition at the genome level is well known to depend on growth temperature (Zeldovich et al, 2007). It is widely acknowledged that the effect of amino acid substitutions on the structural stability of proteins is a major factor affecting amino acid usage in thermophiles (Sterner and Liebl, 2001; Zeldovich et al, 2007). The most common interpretation of these trends is that particular amino acid substitutions are selected through evolution to increase the stability and solubility of the folded conformation and enhance other structural properties such as flexibility (Paul et al, 2008)
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