Intragenomic 16s rDNA divergence in Haloarcula marismortui is an adaptation to different temperatures

Journal of Molecular Evolution

Volumn 65, Issue 6, 2007, Pages 687-696

  Lopez Lopez A ^a,c   Benlloch, S ^b   Bonfa M ^a   Rodriguez Valera F ^a   Mira, A ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO DE ALICANTE   (Spain)

^c CSIC   (Spain)

Author keywords

Concerted evolution; Extremophile; Genome evolution; Paralogues; Phylogenetic marker; Real time PCR; Ribosomal operons; Thermal adaptation; Thermal stability; Thermophile

Indexed keywords

DNA 16S; GENOMIC DNA; RIBOSOME RNA; RNA 16S; RNA 23S; RNA 5S; SODIUM CHLORIDE;

ARTICLE; BIODIVERSITY; CONCENTRATION RESPONSE; ENVIRONMENTAL TEMPERATURE; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE STRUCTURE; GENETIC HETEROGENEITY; GENETIC MARKER; GENETIC POLYMORPHISM; GENETIC STABILITY; GENETIC STRAIN; GENETIC VARIABILITY; HABITAT; HALOARCULA MARISMORTUI; HALOPHILE; HALOPHILIC ARCHAEON; HIGH TEMPERATURE; INCUBATION TEMPERATURE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHYLOGENY; POLYMERASE CHAIN REACTION; PROMOTER REGION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SALT TOLERANCE; TEMPERATURE ACCLIMATIZATION; THERMOPHILE; THERMOSTABILITY;

ADAPTATION, PHYSIOLOGICAL; BASE SEQUENCE; DNA, ARCHAEAL; DNA, RIBOSOMAL; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ARCHAEAL; GENOME, ARCHAEAL; HALOARCULA MARISMORTUI; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; POLYMERASE CHAIN REACTION; RNA STABILITY; RNA, RIBOSOMAL, 16S; RRNA OPERON; SEQUENCE HOMOLOGY, NUCLEIC ACID; TEMPERATURE; VARIATION (GENETICS);

ARCHAEA; HALOARCULA MARISMORTUI;

EID: 37549063435     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-007-9047-3     Document Type: Article

References (43)

1. Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186:2629-2635
2. Amann G, Stetter KO, Llobet-Brossa E, Amann R, Anton J (2000) Direct proof for the presence and expression of two 5% different 16S rRNA genes in individual cells of Haloarcula marismortui. Extremophiles 4:373-376
3. Arndt E, Kromer W, Hatakeyama T (1990) Organization and nucleotide sequence of a gene cluster coding for eight ribosomal proteins in the archaebacterium Halobacterium marismortui. J Biol Chem 265:3034-3039
4. Asai T, Zaporojets D, Squires C, Squires CL (1999) An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc Natl Acad Sci USA 96:1971-1976
5. Baliga NS, Bonneau R, Facciotti MT, Pan M, Glusman G, Deutsch EW, Shannon P, Chiu Y, Weng RS, Gan RR, Hung P, Date SV, Marcotte E, Hood L, Ng WV (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14:2221-2234
6. Baliga NS, DasSarma S (1999) Saturation mutagenesis of the TATA box and upstream activator sequence in the haloarchaeal bop gene promoter. J Bacteriol 181:2513-2518
7. Bao Q, Tian Y, Li W, Xu Z, Xuan Z, Hu S, Dong W, Yang J, Chen Y, Xue Y, Xu Y, Lai X, Huang L, Dong X, Ma Y, Ling L, Tan H, Chen R, Wang J, Yu J, Yang H (2002) A complete sequence of the T. tengcongensis genome. Genome Res 12:689-700
8. Bonete MJ, Perez-Pomares F, Diaz S, Ferrer J, Oren A (2003) Occurrence of two different glutamate dehydrogenase activities in the halophilic bacterium Salinibacter ruber. FEMS Microbiol Lett 226:181-186
9. Boucher Y, Douady CJ, Sharma AK, Kamekura M, Doolittle WF (2004) Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J Bacteriol 186:3980-3990
10. Brochier C, Philippe H (2002) Phylogeny: a non-hyperthermophilic ancestor for bacteria. Nature 417:244
11. Clayton RA, Sutton G, Hinkle PS Jr, Bult C, Fields C (1995) Intraspecific variation in small-subunit rRNA sequences in GenBank: why single sequences may not adequately represent prokaryotic taxa. Int J Syst Bacteriol 45:595-599
12. Coenye T, Vandamme P (2003) Intragenomic heterogeneity between multiple 16S ribosomal RNA operons in sequenced bacterial genomes. FEMS Microbiol Lett 228:45-49
13. Condon C, Squires C, Squires CL (1995) Control of rRNA transcription in Escherichia coli. Microbiol Rev 59:623-645
14. Dennis PP, Ziesche S, Mylvaganam S (1998) Transcription analysis of two disparate rRNA operons in the halophilic archaeon Haloarcula marismortui. J Bacteriol 180:4804-4813
15. Eleaume H, Jabbouri S (2004) Comparison of two standardisation methods in real-time quantitative RT-PCR to follow Staphylococcus aureus genes expression during in vitro growth. J Microbiol Methods 59:363-370
16. Fitzmaurice J, Glennon M, Duffy G, Sheridan JJ, Carroll C, Maher M (2004) Application of real-time PCR and RT-PCR assays for the detection and quantitation of VT 1 and VT 2 toxin genes in E. coli O157:H7. Mol Cell Probes 18:123-132
17. 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, Stuttgart
18. Green R, Noller HF (1997) Ribosomes and translation. Annu Rev Biochem 66:679-716
19. Gunderson JH, Sogin ML, Wollett G, Hollingdale M, de la Cruz VF, Waters AP, McCutchan TF (1987) Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238:933-937
20. Hamacher K, Trylska J, McCammon JA (2006) Dependency map of proteins in the small ribosomal subunit. PLoS Comput Biol 2:e10
21. Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429-3431
22. Karlen Y, McNair A, Perseguers S, Mazza C, Mermod N (2007) Statistical significance of quantitative PCR. BMC Bioinformatics 8:131-146
23. Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328-1333
24. Lauro FM, Chastain RA, Blankenship LE, Yayanos AA, Bartlett DH (2007) The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl Environ Microbiol 73:838-845
25. Martinez-Murcia AJ, Anton AI, Rodriguez-Valera F (1999) Patterns of sequence variation in two regions of the 16S rRNA multigene family of Escherichia coli. Int J Syst Bacteriol 49:601-610
26. Matzura O, Wennborg A (1996) RNAdraw: an integrated program for RNA secondary structure calculation and analysis under 32-bit Microsoft Windows. Comput Appl Biosci 12:247-249
27. Mevarech M, Hirsch-Twizer S, Goldman S, Yakobson E, Eisenberg H, Dennis PP (1989) Isolation and characterization of the rRNA gene clusters of Halobacterium marismortui. J Bacteriol 171:3479-3485
28. 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 13
29. 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 102:18147-18152
30. Mylvaganam S, Dennis PP (1992) Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui. Genetics 130:399-410
31. Pronk LM, Sanderson KE (2001) Intervening sequences in rrl genes and fragmentation of 23S rRNA in genera of the family Enterobacteriaceae. J Bacteriol 183:5782-5787
32. Pushker R, Mira A, Rodriguez-Valera F (2004) Comparative genomics of gene-family size in closely related bacteria. Genome Biol 5:R27
33. 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 187:923-929
34. Soppa J (2005) From replication to cultivation: hot news from Haloarchaea. Curr Opin Microbiol 8:737-744
35. Stetter KO (1996) Hyperthermophiles in the history of life. CIBA Found Symp 202:1-10
36. Torarinsson E, Klenk HP, Garrett RA (2005) Divergent transcriptional and translational signals in Archaea. Environ Microbiol 7:47-54
37. Tu D, Blaha G, Moore PB, Steitz TA (2005) Gene replacement in Haloarcula marismortui: construction of a strain with two of its three chromosomal rRNA operons deleted. Extremophiles 9:427-435
38. Turner DH, Sugimoto N, Jaeger JA, Longfellow CE, Freier SM, Kierzek R (1987) Improved parameters for prediction of RNA structure. Cold Spring Harb Symp Quant Biol 52:123-133
39. Weinberg MV, Schut GJ, Brehm S, Datta S, Adams MW (2005) Cold shock of a hyperthermophilic archaeon: Pyrococcus furiosus exhibits multiple responses to a suboptimal growth temperature with a key role for membrane-bound glycoproteins. J Bacteriol 187:336-348
40. Wuchty S, Fontana W, Hofacker IL, Schuster P (1999) Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers 49:145-165
41. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI (2003) A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299:2074-2076
42. Yang CF, Kim JM, Molinari E, DasSarma S (1996) Genetic and topological analyses of the bop promoter of Halobacterium halobium: stimulation by DNA supercoiling and non-B-DNA structure. J Bacteriol 178:840-845
43. Yap WH, Zhang Z, Wang Y (1999) Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol 181:5201-5209