EVOLUTIONARY DIVERGENCE AND SALINITY-MEDIATED SELECTION IN HALOPHILICARCHAEA

Halophilic (literally salt-loving) archaea are a highly evolved group of organisms that are uniquely able to survive in and exploit hypersal ine environments. In this review, we examine the potential interplay b etween fluctuations in environmental salinity and the primary sequence and tertiary structure of halophilic proteins. The proteins of haloph ilic archaea are highly adapted and magnificently engineered to functi on in an intracellular milieu that is in ionic balance with an externa l environment containing between 2 and 5 M inorganic salt. To understa nd the nature of halophilic adaptation and to visualize this interplay , the sequences of genes encoding the L11, L1, L10, and L12 proteins o f the large ribosome subunit and Mn/Fe superoxide dismutase proteins f rom three genera of halophilic archaea have been aligned and analyzed for the presence of synonymous and nonsynonymous nucleotide substituti ons. Compared to homologous eubacterial genes, these halophilic genes exhibit an inordinately high proportion of nonsynonymous nucleotide su bstitutions that result in amino acid replacement in the encoded prote ins. More than one-third of the replacements involve acidic amino acid residues. We suggest that fluctuations in environmental salinity prov ide the driving force for fixation of the excessive number of nonsynon ymous substitutions. Tinkering with the number, location, and arrangem ent of acidic and other amino acid residues influences the fitness (i. e., hydrophobicity, surface hydration, and structural stability) of th e halophilic protein. Tinkering is also evident at halophilic protein positions monomorphic or polymorphic for serine; more than one-third o f these positions use both the TCN and the AGY serine codons, indicati ng that there have been multiple nonsynonymous substitutions at these positions. Our model suggests that fluctuating environmental salinity prevents optimization of fitness for many halophilic proteins and help s to explain the unusual evolutionary divergence of their encoding gen es.