Molecular Biology and Evolution 18:741-749 (2001)
© 2001 Society for Molecular Biology and Evolution
ARTICLE |
Patterns of Temperature Adaptation in Proteins from the Bacteria Deinococcus radiodurans and Thermus thermophilus
Department of Biological Sciences, University of Delaware
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Abstract |
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Asymmetrical patterns of amino acid substitution in proteins of organisms living at moderate and high temperatures (mesophiles and thermophiles, respectively) are generally taken to indicate selection favoring different amino acids at different temperatures due to their biochemical properties. If that were the case, comparisons of different pairs of mesophilic and thermophilic taxa would exhibit similar patterns of substitutional asymmetry. A previous comparison of mesophilic versus thermophilic Methanococcus with mesophilic versus thermophilic Bacillus revealed several pairs of amino acids for which one amino acid was favored in thermophilic Bacillus and the other was favored in thermophilic Methanococcus. Most of this could be explained by the higher G+C content of the DNA of thermophilic Bacillus, a phenomenon not seen in the Methanococcus comparison. Here, I compared the mesophilic bacterium Deinococcus radiodurans and its thermophilic relative Thermus thermophilus, which are similar in G+C content. Of the 190 pairs of amino acids, 83 exhibited significant substitutional asymmetry, consistent with the pervasive effects of selection. Most of these significantly asymmetrical pairs of amino acids were asymmetrical in the direction predicted from the Methanococcus data, consistent with thermal adaptation resulting from universal biochemical properties of the amino acids. However, 12 pairs of amino acids exhibited asymmetry significantly different from and in the opposite direction of that found in the Methanococcus comparison, and 21 pairs of amino acids exhibited asymmetry that was significantly different from that found in the Bacillus comparison and could not be explained by the greater G+C content in thermophilic Bacillus. This suggests that selection due to universal biochemical properties of the amino acids and differences in G+C content are not the only causes of substitutional asymmetry between mesophiles and thermophiles. Instead, selection on taxon-specific properties of amino acids, such as their metabolic cost, may play a role in causing asymmetrical patterns of substitution.
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionliterature cited |
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Organisms live at a wide range of temperatures, from <0°C to >100°C, and they do so despite the dramatic effects of temperature on the function and stability of their proteins. Understanding how proteins have adapted to different temperatures therefore has long been the subject of considerable research. One approach has been to search for asymmetrical substitution patterns in protein sequences from organisms living at different temperatures, usually prokaryotes living at moderate temperatures (mesophiles) compared with those living at high temperatures (thermophiles) (Argos et al. 1979
; Menéndez-Arias and Argos 1989
; Vogt, Woell, and Argos 1997
; Haney et al. 1999
; McDonald, Grasso, and Rejto 1999
). If protein evolution is largely due to neutral processes, or due to adaptation that is specific to each protein and each site, then the substitutions are expected to be symmetrical: there will be as many aligned sites with amino acid A in the mesophile and amino acid B in the thermophile as there are sites with the opposite pattern. Significant asymmetry, such as a greater number of sites with A in the mesophile and B in the thermophile, is usually interpreted as evidence that selection favors different amino acids at different temperatures, and much effort has been put into trying to identify biochemical properties of the amino acids that would explain this adaptation.
Most of the protein sequence comparisons of mesophiles with thermophiles have examined a small number of proteins from a broad range of organisms (Argos et al. 1979
; Menéndez-Arias and Argos 1989
; Vogt, Woell, and Argos 1997
). Some consistent patterns have been evident, such as arginine being preferred over lysine at higher temperatures, but the broad taxonomic samples have made it difficult to know whether any general patterns of thermal adaptation are being obscured or exaggerated by taxon-specific asymmetries that may or may not be thermally adaptive. Recent whole-genome sequence projects have made it possible to examine a large number of protein sequences from a single pair of mesophilic versus thermophilic taxa. Haney et al. (1999)
compared 115 protein sequences from the mesophilic archaea Methanococcus maripaludis, Methanococcus vannielii, and Methanococcus voltae with the thermophilic Methanococcus jannaschii. They found 26 of the 190 pairs of amino acids to show significant (P < 0.01) asymmetry, suggesting that adaptation to temperature had an effect on a substantial proportion of amino acid substitutions. McDonald, Grasso, and Rejto (1999)
examined a similar data set from the same species of Methanococcus and compared the results with the patterns of asymmetry between the mesophilic bacterium Bacillus subtilis and the thermophilic Bacillus stearothermophilus. The Bacillus comparison displayed significant (P < 0.05) substitutional asymmetry at 54 pairs of amino acids, and most of the asymmetry was consistent in direction with that seen in the Methanococcus comparison. However, several pairs of amino acids showed patterns of asymmetry that were significantly different and opposite in direction in the Methanococcus and Bacillus data sets, suggesting that taxon-specific processes were indeed important. Most of these differences consisted of an amino acid with a more G+C-rich codon being favored in thermophilic Bacillus but less common in thermophilic Methanococcus, consistent with the higher genomic G+C content of B. stearothermophilus compared with B. subtilis. Because mesophilic and thermophilic Methanococcus differ little in genomic G+C content, McDonald, Grasso, and Rejto (1999)
suggested that the asymmetrical substitution patterns seen there gave a better indication of which amino acid substitutions were adaptive at different temperatures.
Even when mesophiles and thermophiles have the same genomic G+C content, it would be hasty to interpret all asymmetrical substitution patterns between them as evidence for thermal adaptation, because there are other processes besides changes in G+C content that could cause taxon-specific patterns of substitutional asymmetry. Amino acids vary in bioenergetic cost, and amino acids with lower costs presumably will be favored over functionally equivalent amino acids (Craig and Weber 1998
; Craig et al. 1999
). The relative bioenergetic costs of different amino acids may vary among species, depending on the availability for uptake of each amino acid in the environment, the biosynthetic pathways used to synthesize each amino acid, the abundance of raw materials for biosynthesis, and the effect of temperature and other environmental variables on the biosynthetic pathways. Environmental variables other than temperature, such as salinity, pH, and hydrostatic pressure, might also cause adaptive substitutional asymmetry that is unrelated to temperature.
Only patterns of substitutional asymmetry that are repeatedly observed in comparisons of mesophiles paired with related thermophiles will be robust evidence for thermal adaptation, while inconsistent patterns of asymmetry could have a variety of possible explanations. Here, I compared sequences from the mesophilic bacterium Deinococcus radiodurans, whose genome has been completely sequenced (White et al. 1999
), with Thermus thermophilus, a thermophilic bacterium that is related to Deinococcus (Hensel et al. 1986
; Weisburg, Giovannoni, and Woese 1989
). The resulting patterns were then compared with those observed earlier in comparisons of mesophilic and thermophilic Methanococcus and Bacillus to determine which asymmetries were consistent and which differed among pairs of species.
Little is known about the natural history of D. radiodurans (Murray 1992
). It can survive remarkable amounts of gamma radiation, which may be a byproduct of adaptation to desiccation resistance (Mattimore and Battista 1996
), and it can also withstand intense ultraviolet radiation (Minton 1994
) and desiccation (Sanders and Maxcy 1979
). Deinococcus radiodurans has a genomic G+C content of 66.6% (White et al. 1999
) and an optimal growth temperature of 25–30°C (Murray 1992
). Thermus thermophilus lives in hot springs and artificial hot water environments. The type strain HB-8, which is used for most sequences, has an optimal growth temperature of 73°C (Williams and da Costa 1992
) and a G+C content of 64.7% (Manaia et al. 1994
). While T. thermophilus is sometimes considered a junior synonym of Thermus aquaticus (Degryse, Glansdorff, and Pierard 1978
), T. thermophilus and T. aquaticus have low similarity in genomic DNA : DNA hybridization (Manaia et al. 1994
; Williams et al. 1995
) and 16s sequences (Saul et al. 1993
), and T. thermophilus can grow in media containing 3% NaCl and has a higher maximum growth temperature than T. aquaticus (Manaia and da Costa 1991
). Here, I compared only T. thermophilus with D. radiodurans, because T. thermophilus has a slightly higher optimum growth temperature and has more sequences publicly available than does T. aquaticus.
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Materials and Methods |
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All available protein sequences (including fragments) for T. thermophilus were downloaded from the SwissProt, TrEMBL, and TrEMBLNew databases in October 2000. Sequences less than 20 amino acids long were discarded. For each sequence, the most similar protein sequence from the complete D. radiodurans genome (White et al. 1999
) was identified using BLAST (Altschul et al. 1997
) servers at the Institute for Genomic Research (http://www.tigr.org/tdb/CMR/gdr/htmls/SeqSearch.html) and the National Center for Biotechnology Information (http://www.ncbi.nlm.nih.gov/blast/blast.cgi). Where more than one sequence from T. thermophilus matched a single sequence in D. radiodurans, presumably reflecting a gene duplication in T. thermophilus or loss of a duplicate in D. radiodurans, only the one sequence with the greatest identity to the D. radiodurans sequence was used. Pairs of amino acid sequences with less than 35% sequence identity were discarded. The resulting data set consisted of 186 sequences from T. thermophilus with matches from D. radiodurans.
Matching sequences were aligned using CLUSTAL W (Thompson, Higgins, and Gibson 1994
). Ambiguously aligned sites adjacent to gaps were omitted, with the omitted sites extending from the gap to the nearest pair of adjacent sites that were both identical in the two sequences. The total data set consisted of 49,337 aligned amino acid sites, of which 18,041 were different between the species. The number of aligned sites exhibiting each of the 190 possible pairwise patterns of difference was then counted. For each pair of amino acids, the significance of the deviation from the expected 50:50 ratio was tested using the log likelihood ratio test (G-test) with the Williams correction for continuity (Sokal and Rohlf 1981
); if the total number of sites was less than 50, Fisher's exact test was used. The ratio for D. radiodurans versus T. thermophilus was compared with the ratio for previously published Bacillus and Methanococcus comparisons (McDonald, Grasso, and Rejto 1999
) using a 2 x 2 contingency table test with the Williams correction (Sokal and Rohlf 1981
); if the total number of sites was less than 50 in either comparison, Fisher's exact test was used.
The information from the 190 pairwise comparisons was summarized into a single ranking of the amino acids from least preferred to most preferred at higher temperatures by assigning a thermal asymmetry index (TAI) reflecting the direction and magnitude of the asymmetries involving that amino acid (McDonald, Grasso, and Rejto 1999
). TAI values were assigned to minimize the difference between the predicted asymmetry for each pair of amino acids (a function of the difference in TAI values) and the observed asymmetry. Because only the difference in TAI values between amino acids was relevant, the TAI values were standardized so that the average value was 1.
To estimate the amount of divergence between pairs of taxa, 17 proteins were identified that were present in the Bacillus, Methanococcus, and Deinococcus/Thermus data sets. The six sequences for each protein were aligned using CLUSTAL W (Thompson, Higgins, and Gibson 1994
), and the sites containing gaps were eliminated. In those sites present in all six species, the proportion of identical sites was calculated for each mesophile-versus-thermophile pair.
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Results |
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For each of the 190 pairs of amino acids, the neutral model predicted an equal number of aligned sites with each direction of difference. There were 19 pairs of amino acids in the Deinococcus/Thermus data set with fewer than six aligned sites, so they could not be significantly asymmetrical at the P < 0.05 level. Of the 171 remaining pairs of amino acids, 83 exhibited significant asymmetry (tables 1–4 ). With this many statistical tests, several were expected to be significant at the P < 0.05 level by chance; after a correction for multiple comparisons (Benjamini and Hochberg 1995
), 64 of these remained significant.
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The patterns of asymmetry could be summarized by assigning each amino acid a TAI (McDonald, Grasso, and Rejto 1999
). These indices were fit to the data such that for each pair of amino acids, the amino acid having a higher index was predicted to be preferred in the thermophile, and the predicted magnitude of the asymmetry was proportional to the difference in the indices. The ordering of amino acids from smallest to largest TAI (fig. 1 ) was consistent with almost all of the significantly asymmetrical pairs; only the preferences in T. thermus of tryptophan over tyrosine and of phenylalanine over tryptophan were not consistent with the ordering based on TAI.
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If the substitutional asymmetry were due to adaptation to different temperatures based solely on the biochemical properties of the amino acids, similar patterns of asymmetry would be expected in pairs of taxa with similar differences in growth temperature. There were 42 pairs of amino acids exhibiting patterns of asymmetry that were significantly different between the Deinococcus/Thermus data set and the Bacillus data set of McDonald, Grasso, and Rejto (1999)
(tables 2 and 3
). Bacillus stearothermophilus had a higher G+C genomic content than B. subtilis, while T. thermophilus had a slightly lower G+C content than D. radiodurans. One might therefore expect stronger asymmetries favoring amino acids with higher G+C content codons in B. stearothermophilus, as seen when the asymmetries in the Bacillus and Methanococcus data sets were compared (McDonald, Grasso, and Rejto 1999
). There were 21 pairs for which the amino acid with greater G+C content was more strongly favored in B. stearothermophilus, and there were only 8 with the opposite pattern (table 2
), suggesting that whatever determines genomic G+C content is affecting the substitutional asymmetries. However, in addition to the eight asymmetries where lower G+C content is favored in B. stearothermophilus, there were 13 asymmetries that did not change the G+C content of the codons and yet showed significantly different asymmetries in the Bacillus and Deinococcus/Thermus data sets (table 3
).
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Mesophilic and thermophilic Methanococcus have similar G+C contents, so if universal biochemical properties and G+C content were the only factors affecting substitutional asymmetry, the patterns would be similar in the Methanococcus data set of McDonald, Rejto, and Grasso (1999)
and the Deinococcus/Thermus data set. If anything, one might expect greater magnitudes of asymmetry in the Methanococcus comparison, since mesophilic and thermophilic Methanococcus have a greater difference in optimal growth temperatures than do D. radiodurans and T. thermophilus. However, of the 22 pairs of amino acids with significantly different patterns of asymmetry in the Methanococcus and Thermus/Deinococcus data sets (table 4
), 12 were asymmetrical in opposite directions in the two pairs of taxa, and 8 were asymmetrical in the same direction but with a greater magnitude of asymmetry in the Deinococcus/Thermus data set. Only the preferences of lysine over serine and of isoleucine over threonine were significantly stronger in the Methanococcus comparison.
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Another way of comparing the patterns of asymmetry between the Methanococcus and Deinococcus/Thermus data sets was to examine the correlation of the thermal asymmetry indices in the two pairs of taxa (fig. 2 ). They were significantly correlated (r2 = 0.60, P < 0.0001), which suggests that the substitutional asymmetry has similar causes in the two pairs of taxa. However, there were four amino acids—isoleucine, cysteine, asparagine, and aspartic acid—that had noticeably lower TAI values in the Deinococcus/Thermus comparison, indicating that they were selected against more strongly in T. thermus than in M. jannaschii. Of the 22 pairs of amino acids that differed significantly in amount of asymmetry between the two pairs of taxa, 14 involved one of these four amino acids being more strongly selected against in T. thermus than in M. jannaschii (table 4 ).
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Because the amount of divergence between a pair of species could affect their patterns of substitutional asymmetry, the divergences between the pairs of mesophilic and thermophilic taxa were estimated. The 17 proteins that were present in all of the Methanococcus, Bacillus, and Deinococcus/Thermus data sets contained 2,576 aligned amino acids after sites aligned with gaps were eliminated. At these sites, there was 64.6% divergence between D. radiodurans and T. thermophilus, 65.7% divergence between the mesophilic Methanococcus and M. jannaschii, and 79.6% divergence between B. subtilis and B. stearothermophilus.
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Discussion |
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Asymmetrical substitution patterns between mesophiles and thermophiles, such as those observed here between D. radiodurans and T. thermophilus and earlier in Methanococcus and Bacillus (Haney et al. 1999
; McDonald, Grasso, and Rejto 1999
), are usually interpreted as evidence for adaptation to different temperatures due to biochemical properties of the amino acids (Argos et al. 1979
; Menéndez-Arias and Argos 1989
; Vogt, Woell, and Argos 1997
; Haney et al. 1999
). If this were the sole cause of asymmetrical substitution, however, the patterns would be similar in all comparisons of mesophiles with thermophiles. There were many pairs of amino acids with consistent patterns of asymmetry in the Bacillus, Methanococcus, and Deinococcus/Thermus comparisons, but there were as many pairs of amino acids with significantly different patterns of asymmetry across the three taxa. This indicates that processes other than selection due to biochemical properties of the amino acids affect the patterns of amino substitution between mesophiles and thermophiles. Here, I review some possible reasons for different patterns of substitutional asymmetry in different pairs of mesophiles and thermophiles.
Difference in G+C Content
While there is no overall correlation of higher G+C content with higher habitat temperature across all prokaryotes (Galtier and Lobry 1997
), thermophiles exhibit higher G+C content than mesophiles within some taxa, such as Bacillus (Claus and Berkeley 1986
) and Methanobacterium (Whitman, Bowen, and Boone 1992
). It is not known whether higher G+C content reflects selection for greater DNA stability or a change in the mutation process (Mooers and Holmes 2000). Organisms with higher G+C content generally have greater abundances of those amino acids with G+C-rich codons (Lobry 1997
and references therein). In the comparison of the mesophile B. subtilis (G+C content 43.5%) with the thermophile B. stearothermophilus (G+C content 52%), the majority of significantly asymmetrical pairs of amino acids favor amino acids with codons with higher G+C content in B. stearothermophilus, while a very small number decrease the G+C content (McDonald, Grasso, and Rejto 1999
). Of the 15 pairs of amino acids that differ significantly in substitution ratio between Methanococcus and Bacillus and are in the opposite direction, all but two have an amino acid with higher G+C content being favored in thermophilic Bacillus and less common in thermophilic Methanococcus. This suggests that some of the asymmetrical substitution patterns observed in Bacillus are due to the differing G+C content of the amino acids' codons, not their biochemical properties. For the Methanococcus and Deinococcus/Thermus comparisons, where the mesophiles and the thermophiles are similar in G+C content, this should not play a major role in producing the asymmetry.
A more subtle way in which G+C content might affect patterns of adaptive asymmetry could result from the differences in the G+C content of the mesophile/thermophile pairs. Imagine a site with amino acid A in a mesophile where either amino acid B or amino acid C would have equally adaptive biochemical properties in a thermophile. If the codons for B have higher G+C content than the codons for C, the A-to-B substitution might be more common in a mesophile/thermophile pair with high G+C content (such as Deinococcus/Thermus), while the A-to-C substitution might be more common in a mesophile/thermophile pair with low G+C content (such as Methanococcus). It will be necessary to compare multiple mesophile/thermophile pairs with similar G+C contents to evaluate the importance of this effect.
Relaxed Constraint
Relaxation of selective constraint such that many sites were constrained to have one amino acid in the ancestral species but could have more than one adaptively equivalent amino acid in one descendant lineage could also lead to asymmetry. Amino acids that increased in frequency in the lineage where they were newly neutral would be difficult to distinguish from those that increased due to positive selection. Because some Deinococcus species (Ferreira et al. 1997
) and all known Thermus species are thermophilic, the common ancestor of the Deinococcus/Thermus group was probably a thermophile, as were the common ancestors of the Methanococcus spp. (Keswani et al. 1996
) and B. subtilis and B. stearothermophilus (Ochi 1994
). If there are many sites with less selective constraint at moderate temperatures than at high temperatures, similar patterns of asymmetry could have arisen in all three comparisons of mesophiles with thermophiles. Comparing a pair of species in which thermophily is the derived state would help to test this possibility.
Unequal Numbers of Mutations
The neutral model yielding symmetrical protein substitution assumes that the numbers of mutations (the number of generations times the mutation rate per generation) are equal on the lineages connecting a mesophile and a thermophile to their common ancestor (McDonald, Grasso, and Rejto 1999
). If there are more generations or more mutations per generation on one lineage than on the other, asymmetrical patterns of substitution may result. There is no evidence for the dramatic difference in substitution rate between mesophiles and thermophiles required for this process to yield asymmetrical substitution patterns. In addition, this process would not change the overall frequencies of the amino acids in proteins, provided that the frequencies of amino acids in the ancestral species were at mutation/drift equilibrium. The significant changes in frequency of several amino acids in the Deinococcus/Thermus (table 5
), Methanococcus, and Bacillus data sets (McDonald, Grasso, and Rejto 1999
) indicate that unequal mutation rates are not the sole cause of the asymmetry.
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Amount of Divergence
If some form of adaptation produces substitutional asymmetry, it is possible to imagine that the more recently diverged of two mesophile-versus-thermophile pairs could exhibit greater asymmetry. At those sites where amino acid A is adaptive at cooler temperatures and amino acid B is adaptive at hotter temperatures, adaptation would occur rapidly after two species split and began living in different temperatures. At those sites where amino acids A and B are functionally equivalent at both high and low temperatures, neutral substitutions in both directions would slowly and symmetrically accumulate. The combination of rapid, asymmetrical substitutions due to adaptation and slow, symmetrical substitutions due to neutral processes would result in higher asymmetry in more recently diverged species.
If the slow accumulation of neutral substitutions were causing different amounts of asymmetry in the different pairs of taxa, one would expect to see more asymmetry in the less diverged pairs of species. Mesophilic Methanococcus and M. jannaschii have about the same amount of divergence (65.7% identity for the 17 proteins analyzed) as D. radiodurans versus T. thermophilus (64.6% identity), so the amount of divergence is unlikely to be the cause of the different patterns of asymmetry in these two comparisons. Bacillus subtilis and B. stearothermophilus reveal considerably less divergence (79.6% identity) than the other mesophile-versus-thermophile comparisons. Of those pairs of amino acids with significantly different asymmetries between the Bacillus and Deinococcus/Thermus data sets that cannot be explained by differences in G+C content, most have less asymmetry in Bacillus than in Methanococcus or Deinococcus/Thermus (table 3 ). Thus, there is no evidence that reduced asymmetry due to slowly accumulating neutral substitutions is important in explaining the differences among the three data sets.
Different Sets of Proteins
It is possible that certain categories of proteins (membrane proteins, highly expressed proteins, ribosomal proteins, enzymes, etc.) exhibit different patterns of adaptive asymmetry from other categories of proteins. A mesophile/thermophile comparison that included mostly proteins from one category could then exhibit different patterns of asymmetry from a mesophile/thermophile comparison including mostly proteins from a different category. None of the three data sets compared here has an obvious preponderance of proteins from one functional category that was rare in one of the other data sets, so it seems unlikely that this is a major cause of the different patterns of asymmetry among the data sets. Detailed examination of the patterns of substitutional asymmetry among functional categories will require much larger data sets for any statistical power.
Selection Due to Environmental Factors Other than Temperature
The environments of mesophiles and thermophiles often differ in other environmental variables; if any of these variables favor some amino acids over others, they might also cause substitutional asymmetry. For example, the mesophilic Methanococcus were isolated from shallow and intertidal marine and estuarine sediments (Stadtman and Barker 1951
; Jones, Paynter, and Gupta 1983
), while the thermophilic M. jannaschii was isolated from a depth of 2,600 m (Jones et al. 1983
). Salinity, hydrostatic pressure, pH, and the abundance of different amino acids and their precursors in the environment are among the environmental variables that could cause selection favoring different amino acids in different environments. To identify those asymmetries caused by temperature differences, one ideally would want to compare two species whose environments are identical except for temperature. Realistically, it will be necessary to compare a large number of mesophile/thermophile pairs, so that temperature is the only environmental variable that consistently differs between them and could therefore explain any consistent asymmetries.
Selection Due to Bioenergetic Costs of the Amino Acids
In addition to biochemical properties and the G+C content of their codons, amino acids differ in their cost of uptake or synthesis, and if these bioenergetic costs vary among species, substitutional asymmetry could result (Craig and Weber 1998
; Craig et al. 1999
). For example, the mesophilic M. voltae lives in marine muds rich in organic material (Whitman et al. 1986
), assimilates all amino acids tested (Ekiel, Jarrell, and Sprott 1985
), and is heterotrophic for leucine and isoleucine (Whitman, Ankwanda, and Wolfe 1982
); presumably, it obtains much of its amino acids from its environment. The thermophile M. jannaschii is autotrophic and has limited ability to assimilate amino acids (Sprott, Ekiel, and Patel 1993
). At sites in protein sequences where two or more amino acids are functionally equivalent, the one that was most abundant in its environment presumably would be favored in M. voltae, while the one with the lowest cost of biosynthesis would be favored in M. jannaschii. This could appear to be temperature-related substitutional asymmetry, although the adaptation might not be caused by the temperature difference.
To summarize, the dramatic substitutional asymmetries observed between proteins from mesophiles and thermophiles are inconsistent with a simple neutral model of protein evolution, but they may not all be the result of temperature adaptation due to biochemical properties of the amino acids. The significant differences among taxa in amount and direction of asymmetry suggest that other processes, such as adaptation to environmental variables other than temperature, selection based on bioenergetic costs of amino acids, or (for taxa such as Bacillus) changes in G+C content, play an important role. As more data become available, those patterns of asymmetry that remain consistent across pairs of mesophiles/thermophiles will become more definitely related to temperature adaptation.
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Footnotes |
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Julian Adams, Reviewing Editor
1 Keywords: protein adaptation
thermophile
Deinococcus
Thermus. 
2 Address for correspondence and reprints: John H. McDonald, Department of Biological Sciences, University of Delaware, Newark, Delaware 19716. mcdonald{at}udel.edu
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