Amino Acid Substitutions in Cold-Adapted Proteins from Halorubrum lacusprofundi, an Extremely Halophilic Microbe from Antarctica

Abstract

The halophilic Archaeon Halorubrum lacusprofundi, isolated from the perennially cold and hypersaline Deep Lake in Antarctica, was recently sequenced and compared to 12 Haloarchaea from temperate climates by comparative genomics. Amino acid substitutions for 604 H. lacusprofundi proteins belonging to conserved haloarchaeal orthologous groups (cHOGs) were determined and found to occur at 7.85% of positions invariant in proteins from mesophilic Haloarchaea. The following substitutions were observed most frequently: (a) glutamic acid with aspartic acid or alanine; (b) small polar residues with other small polar or non-polar amino acids; (c) small non-polar residues with other small non-polar residues; (d) aromatic residues, especially tryptophan, with other aromatic residues; and (e) some larger polar residues with other similar residues. Amino acid substitutions for a cold-active H. lacusprofundi β-galactosidase were then examined in the context of a homology modeled structure at residues invariant in homologous enzymes from mesophilic Haloarchaea. Similar substitutions were observed as in the genome-wide approach, with the surface accessible regions of β-galactosidase displaying reduced acidity and increased hydrophobicity, and internal regions displaying mainly subtle changes among smaller non-polar and polar residues. These findings are consistent with H. lacusprofundi proteins displaying amino acid substitutions that increase structural flexibility and protein function at low temperature. We discuss the likely mechanisms of protein adaptation to a cold, hypersaline environment on Earth, with possible relevance to life elsewhere.

Carbon monoxide as a metabolic energy source for extremely halophilic microbes: Implications for microbial activity in Mars regolith

“…However, significant CO uptake likely occurs at even lower temperatures in other halophiles, because Octadecabacter antarcticus 307, a marine psychrophile with form I genes for CO oxidation, grows at 4°C or lower in brines with at least twice the salinity of full-strength seawater (41). Extreme halophiles have also been isolated from and are active in subzero Antarctic and Arctic brines (42)(43)(44)(45)(46)(47)(48). In addition, atmospheric CO uptake has been documented for Maine forest soils incubated at 0°C (35), which indicates that cold-tolerant CO-oxidizing populations might be widely distributed, and provides important insights about the behavior of extraterrestrial systems, such as the RSL, that experience large seasonal shifts in temperature.…”

Protein Adaptations in Archaeal Extremophiles

“…As an example of these features, proteins from the archaeal cold-adapted halophile Halorubum lacusprofundi display a decrease in large hydrophobic amino acids, such as tryptophan, and in hydrogen bond forming residues, like glutamic acid. In the H. lacusprofundiβ -galactosidase, there was an increasing hydrophobicity observed on the protein surface, which replaced anionic electrostatic interactions which are usually abundant on halophilic proteins [68, 69]. These types of amino acid trends have also been reported in the elongation factor 2 proteins of psychrophilic methanogens [70].…”

Some like it cold: understanding the survival strategies of psychrophiles

“…Similarly, comparative analyses of Halobacterium sp. tADL isolated from Deep Lake in Antarctica showed unique genomic features, including gas vesicle, bacteriorhodopsin and polyhydroxyalkanoate biosynthesis genes, which may contribute to its dominance in this environment , whereas a comparison of the Antarctic halophilic archaeon Halorubrumlacus profundi with various mesophilic haloarchaea showed amino acid substitutions in 7.85% of positions in H. lacusprofundi proteins invariant in the mesophiles .…”