Prokaryotes that grow optimally in acid have purine-poor codons in long open reading frames

Area of Science:

• Microbiology
• Molecular Biology
• Genetics

Background:

• Nucleic acids, specifically N-glycosyl bonds in purines, are susceptible to degradation under acidic conditions.
• The archaeon Picrophilus torridus thrives in extremely acidic environments (pH near zero) and high temperatures (near 60°C).
• Thermophiles typically utilize purine-rich codons to enhance DNA stability at high temperatures.

Purpose of the Study:

• To investigate the adaptive strategies of Picrophilus torridus concerning its DNA composition in response to extreme pH and temperature.
• To determine how codon usage in P. torridus balances the conflicting requirements of thermophily and acidophily.
• To explore the relationship between open reading frame length, purine content, and potential mutational vulnerability.

Main Methods:

• Analysis of codon usage bias in the genome of Picrophilus torridus.
• Correlation of codon composition with optimal growth temperature and pH.
• Examination of purine and pyrimidine content in relation to open reading frame lengths.

Main Results:

• P. torridus exhibits increased use of purine-rich codons, consistent with adaptation to high temperatures, with extra purines often located in non-amino acid-determining codon positions.
• As open reading frame lengths increase, there is a shift towards purine-poor codons, particularly those lacking purines in amino acid-determining positions, indicating adaptation to acidic conditions.
• Longer open reading frames, representing larger targets for depurination, appear to have evolved reduced purine content, potentially through pyrimidine substitutions, to mitigate acid-induced mutations.

Conclusions:

• Picrophilus torridus employs a dual strategy to adapt its genome: increasing purines to favor thermophilic codon usage without significantly altering protein sequences, and decreasing purines in longer open reading frames to enhance acid resistance.
• The observed codon usage patterns suggest a mechanism for reducing mutational susceptibility in longer DNA segments under extreme pH conditions.
• This study highlights the intricate interplay between environmental adaptation and genomic composition in extremophilic archaea.