Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii

Abstract

We generated draft genome sequences for two cold-adapted Archaea, Methanogenium frigidum and Methanococcoides burtonii, to identify genotypic characteristics that distinguish them from Archaea with a higher optimal growth temperature (OGT). Comparative genomics revealed trends in amino acid and tRNA composition, and structural features of proteins. Proteins from the cold-adapted Archaea are characterized by a higher content of noncharged polar amino acids, particularly Gln and Thr and a lower content of hydrophobic amino acids, particularly Leu. Sequence data from nine methanogen genomes (OGT 15 degrees -98 degrees C) were used to generate 1111 modeled protein structures. Analysis of the models from the cold-adapted Archaea showed a strong tendency in the solvent-accessible area for more Gln, Thr, and hydrophobic residues and fewer charged residues. A cold shock domain (CSD) protein (CspA homolog) was identified in M. frigidum, two hypothetical proteins with CSD-folds in M. burtonii, and a unique winged helix DNA-binding domain protein in M. burtonii. This suggests that these types of nucleic acid binding proteins have a critical role in cold-adapted Archaea. Structural analysis of tRNA sequences from the Archaea indicated that GC content is the major factor influencing tRNA stability in hyperthermophiles, but not in the psychrophiles, mesophiles or moderate thermophiles. Below an OGT of 60 degrees C, the GC content in tRNA was largely unchanged, indicating that any requirement for flexibility of tRNA in psychrophiles is mediated by other means. This is the first time that comparisons have been performed with genome data from Archaea spanning the growth temperature extremes from psychrophiles to hyperthermophiles.

Figure 1

Multiple alignment (CLUSTALW) of archaeal Csp sequences. (^*) Conserved residues in M. frigidum Csp involved with RNA binding.

Figure 2

PCA of amino acid composition in archaeal proteomes. (A) Component scores for organisms; (B) component loadings for amino acids. af, Archaeoglobus fulgidus; ap, Aeropyrum pernix; fa, Ferroplasma acidarmanus; halo, Halobacterium sp. NRC-1; ma, Methanosarcina acetivorans; mbar, Methanosarcina barkeri; mbur, Methanococcoides burtonii; mf, Methanogenium frigidum; mj, Methanocaldococcus jannaschii; mk, Methanopyrus kandleri; mm, Methanosarcina mazei; mmar, Methanococcus maripaludis; mt, Methanobacter thermautotrophicus; pa, Pyrobaculum aerophilum; pab, Pyrococcus abyssi; pf, Pyrococcus furiosus; ph, Pyrococcus horikoshii; ss, Sulfolobus solfataricus; st, Sulfolobus tokodaii; ta, Thermoplasma acidophilum; tv, Thermoplasma volcanium.

Figure 3

Contribution of amino acids to the surfaces of modeled proteins from methanogens. (A) Mean fraction of solvent-accessible (▪) and buried (□) surface that is charged residues. (B) Mean fraction of solvent-accessible surface that is hydrophobic residues. (C) Mean fraction of solvent-accessible (▪) and buried (□) surface that is Gln. (D) Mean fraction of solvent-accessible (▪) and buried (□) surface that is Thr. Error bars are standard error of the mean (s.e.m.).

Figure 4

Mean GC fraction of predicted tRNA sequences from archaeal genomes. Total GC (□), stem GC (○). Error bars: s.e.m.