Abstract
In nucleic acids the N-glycosyl bonds between purines and their ribose sugar moities are broken under acid conditions. If one strand of a duplex DNA segment were more vulnerable to mutation than the other, then the archaeon Picrophilus torridus, with an optimum growth pH near zero, could have adapted by decreasing the purine content of that strand. Yet, P. torridus has an optimum growth temperature near 60 degrees C, and thermophiles prefer purine-rich codons. We found that, as in other thermophiles, high growth temperature correlates with the use of purine-rich codons. The extra purines are often in third, non-amino acid determining, codon positions. However, as in other acidophiles, as open reading frame lengths increase, there is increased use of purine-poor codons, particularly those without purines in second, amino acid-determining, codon positions. Thus, P. torridus can be seen as adapting (a) to temperature by increasing its purines in all open reading frames without greatly impacting protein amino acid compositions, and (b) to pH by decreasing purines in longer open reading frames, thereby potentially impacting protein amino acid compositions. It is proposed that longer open reading frames, being larger mutational targets, have become less vulnerable to depurination by virtue of pyrimidine for purine substitutions.
MeSH Terms
Adaptation, Physiological
Archaeal Proteins/genetics,metabolism
Base Composition
Codon/metabolism
DNA, Archaeal/metabolism
Evolution, Molecular
Gene Expression Regulation, Archaeal
Hydrogen-Ion Concentration
Mutation
Open Reading Frames
Purines/metabolism
Temperature
Thermoplasmales/genetics,growth & development,metabolism
Chemicals
Archaeal Proteins
Codon
DNA, Archaeal
Purines
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lin Feng-Hsu
Department of Biochemistry, Queen's University, K7L3N6, Kingston, ON, Canada.
Forsdyke Donald R
References (35)
35 references, click to expand
-
Alkalithermophiles.
Biochem Soc Trans. 2004 Apr;32(Pt 2):193-8
PMID: 15046570
-
Codon usage tabulated from international DNA sequence databases: status for the year 2000.
Nucleic Acids Res. 2000 Jan 1;28(1):292
PMID: 10592250
-
Comparison of responses by bacteriophages and bacteria to pressures on the base composition of open reading frames.
Appl Bioinformatics. 2003;2(1):47-62
PMID: 15130833
-
Chargaff's legacy.
Gene. 2000 Dec 30;261(1):127-37
PMID: 11164044
-
Immunity as a function of the unicellular state: implications of emerging genomic data.
Trends Immunol. 2002 Dec;23(12):575-9
PMID: 12464568
-
Investigation on the causes of codon and amino acid usages variation between thermophilic Aquifex aeolicus and mesophilic Bacillus subtilis.
J Biomol Struct Dyn. 2004 Oct;22(2):205-14
PMID: 15317481
-
Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0.
J Bacteriol. 1995 Dec;177(24):7050-9
PMID: 8522509
-
Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli.
Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13919-24
PMID: 8943036
-
Transproteomic evidence of a loop-deletion mechanism for enhancing protein thermostability.
J Mol Biol. 1999 Jul 9;290(2):595-604
PMID: 10390356
-
PGTdb: a database providing growth temperatures of prokaryotes.
Bioinformatics. 2004 Jan 22;20(2):276-8
PMID: 14734322
-
Self-catalyzed site-specific depurination of guanine residues within gene sequences.
Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4392-7
PMID: 16537362
-
Another extreme genome: how to live at pH 0.
Trends Microbiol. 2005 Feb;13(2):49-51
PMID: 15680761
-
Empirical analysis of protein insertions and deletions determining parameters for the correct placement of gaps in protein sequence alignments.
J Mol Biol. 2004 Aug 6;341(2):617-31
PMID: 15276848
-
Amino acids as placeholders: base-composition pressures on protein length in malaria parasites and prokaryotes.
Appl Bioinformatics. 2005;4(2):117-30
PMID: 16128613
-
How do thermophilic proteins deal with heat?
Cell Mol Life Sci. 2001 Aug;58(9):1216-33
PMID: 11577980
-
The stability of proteins in extreme environments.
Curr Opin Struct Biol. 1998 Dec;8(6):738-48
PMID: 9914256
-
Optimum growth temperature and the base composition of open reading frames in prokaryotes.
Extremophiles. 2003 Dec;7(6):443-50
PMID: 14666404
-
Evolution of the mitochondrial genetic system: an overview.
Gene. 2000 Dec 30;261(1):153-9
PMID: 11164046
-
Compositional correlation between deoxyribonucleic acid and protein.
Cold Spring Harb Symp Quant Biol. 1961;26:35-43
PMID: 13918160
-
The correlation between genomic G+C and optimal growth temperature of prokaryotes is robust: a reply to Marashi and Ghalanbor.
Biochem Biophys Res Commun. 2005 May 6;330(2):357-60
PMID: 15796890
-
A relationship between GC content and coding-sequence length.
J Mol Evol. 1996 Sep;43(3):216-23
PMID: 8703087
-
Double-stranded RNA as a not-self alarm signal: to evade, most viruses purine-load their RNAs, but some (HTLV-1, Epstein-Barr) pyrimidine-load.
J Theor Biol. 2001 Feb 21;208(4):475-91
PMID: 11222051
-
On the origin of genomic adaptation at high temperature for prokaryotic organisms.
Biochem Biophys Res Commun. 2005 May 13;330(3):629-32
PMID: 15809043
-
Genomic GC content prediction in prokaryotes from a sample of genes.
Gene. 2005 Sep 12;357(2):137-43
PMID: 16125339
-
Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Picrophilus oshimae.
Extremophiles. 1998 May;2(2):67-74
PMID: 9672680
-
X-ray structures of the maltose-maltodextrin-binding protein of the thermoacidophilic bacterium Alicyclobacillus acidocaldarius provide insight into acid stability of proteins.
J Mol Biol. 2004 Jan 2;335(1):261-74
PMID: 14659755
-
Genomic correlates of hyperthermostability, an update.
J Biol Chem. 2003 May 9;278(19):17198-202
PMID: 12600994
-
Internal correspondence analysis of codon and amino-acid usage in thermophilic bacteria.
J Appl Genet. 2003;44(2):235-61
PMID: 12817570
-
Adaptive role of increased frequency of polypurine tracts in mRNA sequences of thermophilic prokaryotes.
Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2951-6
PMID: 14973185
-
Dual information in DNA and the evolution of the genetic code.
J Theor Biol. 1971 Aug;32(2):293-8
PMID: 5566788
-
Thermophilic bacteria strictly obey Szybalski's transcription direction rule and politely purine-load RNAs with both adenine and guanine.
Genome Res. 2000 Feb;10(2):228-36
PMID: 10673280
-
Genome sequence of Picrophilus torridus and its implications for life around pH 0.
Proc Natl Acad Sci U S A. 2004 Jun 15;101(24):9091-6
PMID: 15184674
-
Protein surface amino acid compositions distinctively differ between thermophilic and mesophilic bacteria.
J Mol Biol. 2001 Jun 15;309(4):835-43
PMID: 11399062
-
The formation apurinic acid from the desoxyribonucleic acid of calf thymus.
J Biol Chem. 1952 Mar;195(1):49-63
PMID: 14938354
-
Evolution of assisted protein folding: the distribution of the main chaperoning systems within the phylogenetic domain archaea.
Front Biosci. 2004 May 01;9:1318-32
PMID: 14977547