Intragenomic 16S rDNA Divergence in Haloarcula marismortui Is an Adaptation to Different Temperatures
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The halophilic archaeon Haloarcula marismortui contains three ribosomal RNA operons, designated rrnA, rrnB, and rrnC. Operons A and C are virtually identical, whereas operon B presents a high divergence in nucleotide sequence, having up to 135 nucleotide polymorphisms among the three 16S, 23S, and 5S ribosomal RNA genes. Quantitative PCR and structural analyses have been performed to elucidate whether the presence of this intragenomic heterogeneity could be an adaptation to the variable environmental conditions in the natural habitat of H. marismortui. Variation in salt concentration did not affect expression but variation in incubation temperature did produce significant changes, with operon B displaying an expression level four times higher than the other two together at 50°C and three times lower at 15°C. We show that the putative promoter region of operon B is also different. In addition, the predicted secondary structure of these genes indicated that they have distinct stabilities at different temperatures and a mutant strain lacking operon B grew slower at high temperatures. This study supports the idea that divergent rRNA genes can be adaptive, with different variants being functional under different environmental conditions (e.g., temperature). The same phenomenon could take place in other halophiles or thermophiles with intragenomic rDNA heterogeneity, where the use of 16S rDNA as a phylogenetic marker and indicator of biodiversity should be used with caution.
KeywordsGenome evolution Ribosomal operons Concerted evolution Thermal adaptation Extremophile Thermophile Paralogues Thermal stability Phylogenetic marker Real-time PCR
This work was funded by the MIRACLE (EVK3-2002-00087) and GEMINI (QLK3-CT-2002-02056) projects of the European Commission. A.M. is funded by a Ramón y Cajal contract from the Ministry of Science and Technology and M.B. by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil). We thank P. B. Moore for kindly providing the mutant strains DT29, DT38, and DT41.
- Garret RA, Aagaard C, Andersen M, Dalgaard JZ, Lykke-Andersen J, Phan HTN, Trevisanato S, Østergaard L, Larsen N, Leffers H (1994) Archaeal rRNA operons, intron splicing and homing endonucleases, RNA polymerase operons and phylogeny. Gustav Fischer Verlag, StuttgartGoogle Scholar
- Mira A, Pushker R (2007) Evolution of genome architecture and the evolution of bacterial pathogens. In: Baquero F, Nombela C, Cassell GH (eds) Introduction to evolutionary biology of bacterial and fungal pathogens. ASM Press, Washington, DC, Chap 13Google Scholar
- Mongodin EF, Nelson KE, Daugherty S, Deboy RT, Wister J, Khouri H, Weidman J, Walsh DA, Papke RT, Sanchez Perez G, Sharma AK, Nesbo CL, MacLeod D, Bapteste E, Doolittle WF, Charlebois RL, Legault B, Rodriguez-Valera F (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci USA 102:18147–18152PubMedCrossRefGoogle Scholar
- Robinson JL, Pyzyna B, Atrasz RG, Henderson CA, Morrill KL, Burd AM, Desoucy E, Fogleman RE 3rd, Naylor JB, Steele SM, Elliott DR, Leyva KJ, Shand RF (2005) Growth kinetics of extremely halophilic archaea (family halobacteriaceae) as revealed by arrhenius plots. J Bacteriol 187:923–929PubMedCrossRefGoogle Scholar