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Low rates of replication errors in chromosomal genes ofSulfolobus spp. demonstrate that these extreme thermoacidophiles can maintain genome integrity in environments with high temperature and low pH. In contrast to this genetic stability, we observed unusually frequent mutation of the β-d -glycosidase gene (lacS ) of a shuttle plasmid (pJlacS ) propagated inSulfolobus acidocaldarius . The resulting Lac− mutants also grew faster than the Lac+ parent, thereby amplifying the impact of the frequentlacS mutations on the population. We developed a mutant accumulation assay and corrections for the effects of copy number and differential growth for this system; the resulting measurements and calculations yielded a corrected rate of 5.1 × 10−4 mutational events at thelacS gene per plasmid replication. Analysis of independentlacS mutants revealed three types of mutations: (i) G·C-to-A·T transitions, (ii) slipped-strand events, and (iii) deletions. These mutations were frequent in plasmid-bornelacS expressed at a high level but not in single-copylacS in the chromosome or at lower levels of expression in a plasmid. Substitution mutations arose at only two of 12 potential priming sites of the DNA primase of the pRN1 replicon, but nearly all these mutations created nonsense (chain termination) codons. The spontaneous mutation rate of plasmid-bornelacS was 175-fold higher under high-expression than under low-expression conditions. The results suggest that important DNA repair or replication fidelity functions are impaired or overwhelmed in pJlacS , with results analogous to those of the “transcription-associated mutagenesis” seen in bacteria and eukaryotes.

Endogenous Mutagenesis in Recombinant Sulfolobus Plasmids