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Identification of Microorganisms by PCR Amplification and Sequencing of a Universal Amplified Ribosomal Region Present in Both Prokaryotes and Eukaryotes

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Identification of Microorganisms by PCR Amplification and Sequencing of a Universal Amplified Ribosomal Region Present in Both Prokaryotes and Eukaryotes Journal of Microbiological Methods 56 (2004) 413–426 www.elsevier.com/locate/jmicmeth Identification of microorganisms by PCR amplification and sequencing of a universal amplified ribosomal region present in both prokaryotes and eukaryotes Rau´l Rivas, Encarna Vela´zquez*, Jose´ Luis Zurdo-Pin˜eiro, Pedro F. Mateos, Eustoquio Martı´nez Molina Departamento de Microbiologı´a y Gene´tica, Universidad de Salamanca, Edificio Departamental de Biologı´a, Campus Miguel de Unamuno, 37007 Salamanca, Spain Received 30 June 2003; received in revised form 11 November 2003; accepted 12 November 2003 Abstract The small ribosomal subunit contains 16S rRNA in prokaryotes and 18S rRNA in eukaryotes. Even though it has been known that some small ribosomal sequences are conserved in 16S rRNA and 18S rRNA molecules, they have been used separately for taxonomic and phylogenetic studies. Here, we report the existence of two highly conserved ribosomal sequences in all organisms that allow the amplification of a zone containing approximately 495 bp in prokaryotes and 508 bp in eukaryotes which we have named the ‘‘Universal Amplified Ribosomal Region’’ (UARR). Amplification and sequencing of this zone is possible using the same two universal primers (U1F and U1R) designed on the basis of two highly conserved ribosomal sequences. The UARR encompasses the V6, V7 and V8 domains from SSU rRNA in both prokaryotes and eukaryotes. The internal sequence of this zone in prokaryotes and eukaryotes is variable and the differences become less marked on descent from phyla to species. Nevertheless, UARR sequence allows species from the same genus to be differentiated. Thus, by UARR sequence analysis the construction of universal phylogenetic trees is possible, including species of prokaryotic and eukaryotic microorganisms together. Single isolates of prokaryotic and eukaryotic microorganisms from different sources can be identified by amplification and sequencing of UARR using the same pair of primers and the same PCR and sequencing conditions. D 2003 Elsevier B.V. All rights reserved. Keywords: Taxonomy; Phylogeny; PCR; Sequencing; Ribosomal RNA 1. Introduction Abbreviations: ATCC; American type culture collection; DSM; German collection of microorganisms; CBS; Centraal Bureau voor All known microorganisms are included in three Schimmelcultures; IFO; Institute for Fermentation of Osaka; CECT; domains: eukarya, archaea and bacteria (Woese et al., Coleccio´n Espan˜ola de Cultivos Tipo. 1990; Doolittle, 1999). The classification within each * Corresponding author. Tel.: +34-923-294532; fax: +34-923- 224876. domain is based in different phenotypic and molec- E-mail address: [email protected] (E. Vela´zquez). ular criteria. Advances in techniques such as PCR 0167-7012/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.mimet.2003.11.007 414 R. Rivas et al. / Journal of Microbiological Methods 56 (2004) 413–426 and DNA sequencing have provided a phylogenetic several procedures to identify eukaryotic microorgan- classification of microorganisms allowing a more isms based on 18S rRNA have been recently reported rapid and reliable identification. Since the works of (Bialek et al., 2002; Booton et al., 2002; Sims et al., Woese concerning evolution (Woese, 1987; Olsen 2002; Radwanska et al., 2002; Sturbaum et al., 2002; and Woese, 1993), ribosomal RNAs are the mole- Vanittanakom et al., 2002; Gatei et al., 2003; Hayden cules most widely employed in phylogenetic studies, et al., 2003). although 16S rRNA—in prokaryotes—and 18S In 1987, Woese wrote ‘‘it is reasonable for a rRNA—in eukaryotes—are used separately in taxo- properly equipped laboratory in the future to sequence nomic studies of these organisms. For several years, on the order of 100 16S rRNA per year’’. Currently, 16S rRNA has been sequenced in most prokaryotes using the new automatic sequencers, this number of and the importance of this molecule grew up since its sequences can be readily obtained in a week. More- use in current phylogenetic classification of prokar- over, the amplification of ribosomal sequences by yotes of the Second Edition of Bergey’s Manual of PCR, the purification—by centrifugation—of the Systematic Bacteriology whose guidelines have been bands obtained and the sequencing– by automatic included in the Web page http://server.mph.msu.edu/ sequencers—of the small ribosomal subunit is easy, bergeys/. Currently, the sequencing of 16S rRNA rapid and reliable. Although many molecular techni- must be performed before the description of any ques have been described after PCR discovery to bacterial species. Moreover, the identification of differentiate microorganisms, the ribosomal sequences bacteria, especially fastidious species, in human, have an important advantage, they are available in animal and plant tissues is one of the most important public databases. The automatic sequencing is a tech- applications of the 16S rRNA molecule in clinical nique that can be routinely performed in many labo- diagnosis. Since the beginning of the 16S rRNA ratories, but the complete 16S rDNA and 18S rDNA sequencing, many works have been performed in sequencing is not a suitable method for rapid identifi- which the use of this molecule in phylogeny of cation because these genes are too large, their sequenc- animal pathogen bacteria is described (Weisburg et ing needs many different primers and it is necessary to al., 1989, 1991) and recently several PCR-based know whether the isolate is a prokaryote or a eukaryote methods have been reported to identify bacteria for before performing the amplification. clinical and veterinary diagnosis (Ley et al., 1998; In this work, we describe a procedure to identify Pusterla et al., 2000; Rantakokko-Jalava et al., 2000; any prokaryotic or eukaryotic microorganism by Dore et al., 2001; Bohr et al., 2002; Chae et al., 2002; sequencing a ‘‘Universal Amplified Ribosomal Re- Lachnik et al., 2002; Millar et al., 2002; Rothman et gion (UARR)’’ from their small ribosomal subunit al., 2002; Yang et al., 2002; Aoki et al., 2003; Bader using the same pair of primers. This procedure et al., 2003; Harris and Hartley, 2003; Riggio and could be applied in the future to identify microbial Lennon, 2003; Saravolatz et al., 2003). In addition, species isolated from environmental and clinical bacteria may be detected by direct PCR using primers sources. targeting 16S rRNA on plant samples (Davis et al., 1997; Lee et al., 1997; Davis et al., 1998; Hauben et al., 1998; Jung et al., 2003; Rodrigues et al., 2003; 2. Material and methods Verdin et al., 2003). Most of these techniques can only detect the species for which the primers and 2.1. Construction of phylogenetic trees probes were designed, but they allow the identifica- tion even when more than one bacterial species is The sequences of 44 representative species of present in the samples. several phyla of archaea, bacteria and eukarya were The 18S rRNA molecule has been also sequenced used (Table 1A and B). We have arranged the in microbial eukaryotes, although it has not yet bacterial and archaeal species in orders and families attained the renown of 16S rDNA in prokaryotes. according to the Second Edition of Bergey’s Manual Nevertheless, many 18S rDNA sequences of eukary- of Systematic Bacteriology whose guidelines have otic species are currently available in databases and been included in the Web page http://server. R. Rivas et al. / Journal of Microbiological Methods 56 (2004) 413–426 415 mph.msu.edu/bergeys/). For the yeast species, we 2.3. Identification of bacteria isolated from legume used the new classification of Kurtzman and Fell nodules using UARR sequencing (1998) and for the filamentous fungi, the Dictionary of the Fungi (Hawksworth et al., 1995). A total of 12 isolates from different legume The sequences were aligned using the ClustalX plants growing in soils from Spain were used. software (Thompson et al., 1997) to find the con- Isolation of strains was made according to Vincent served regions in 16S rDNA and 18S rDNA. Two (1970) using yeast manitol agar, YMA (Bergersen, universal primers were designed based on these 1961). For DNA extraction, the strains were incu- sequences (U1F and U1R) to amplify UARR. To bated in tryptone-yeast agar, TY (Beringer, 1974) at analyse the phylogenetic relationships among the 28 jC and 180 rpm for 24 h the fast growing UARR of the species, the distances were calculated isolates and for 72 h the slow growing isolates. according to Kimura’s two-parameter method DNA was extracted as has been previously reported (Kimura, 1980). Phylogenetic trees were inferred (Rivas et al., 2001). using parsimony (Felsenstein, 1983). Bootstrap anal- ysis was based on 1000 resamplings. The MEGA 2 2.4. Detection of bacterial species in tissues from package (Kumar et al., 2001) was used for all eukaryotic organisms analyses. The reliability of the primers U1F and U1R to detect 2.2. Microbial strains and culture conditions bacteria in tissues from eukaryotic organisms was tested in tissues of uninfected Nicotiana plants and in The strains used are listed in Table 1C. The follow- spleen and liver samples of healthy mice. A human ing type strains from different prokaryotic and eukary- blood sample, in which we have spiked a suspension of otic species were used: Escherichia coli ATCC11775T, E. coli in DEPC-treated water, was also used. Rhizobium tropici CIAT899T, Rhizobium leguminosa- The contaminant DNA from the PCR reagents was rum ATCC10004T, Brevundimonas diminuta eliminated using the protocol described by Rothman et ATCC11568T, Lactobacillus casei DSM20021T, Clav- al. (2002). Alternatively, the restriction enzyme AluI ibacter michiganensis DSM46364T, Streptomyces gri- was substituted by DNAse which was inactivated at seus ATCC23345T, Haloarcula hispanica 121 jC (in autoclave) during 5–8 min. In this case only T ATCC33960 , Halobacterium salinarium the water, the commercial buffer and the MgCl2 solu- ATCC33171T, Halococcus morrhuae ATCC 17082T, tion were separately treated and inactivated. These Saccharomyces cerevisiae CBS1171T, Rhodotorula reagents were aliquoted and maintained at À 20 jC mucilaginosa CBS330T and Hypocrea lutea until their use.
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