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1 Genetic Resources Division, National Institute of Agricultural Biotechnology, Suwon 441-707, Korea
2 Crop Protection Laboratory, National Jeju Agricultural Experiment Station, Jeju 690-150, Korea
3 Department of Forest Resources, Seoul National University, Suwon 441-744, Korea
4 Department of Biological Science, Myong Ji University, Yongin 449-728, Korea
Correspondence
Joo-Won Suh
jwsuh{at}mju.ac.kr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 12 September 2003 as DOI 10.1099/ijs.0.02624-0.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Plant-pathogenic Streptomyces species cause diseases of diverse root crops such as potato, radish, turnip, beet, carrot and sweet potato (Labeda & Lyons, 1992; Goyer & Beaulieu, 1997). Scab diseases of potatoes and other root crops, except sweet potato, are characterized by corky lesions which may appear as shallow, raised or deep pitted lesions on potato tubers and expanded tap roots and cause economically significant losses in yield (Loria et al., 1997). These diseases are known to be caused by Streptomyces scabiei (Lambert & Loria, 1989a; Trüper & Clari, 1997), Streptomyces acidiscabies (Lambert & Loria, 1989b), Streptomyces turgidiscabies (Miyajima et al., 1998) and other species (Faucher et al., 1995; Goyer et al., 1996; Bouchek-Mechiche et al., 2000). Streptomyces scabiei is the predominant causal agent and most closely related to the Diastatochromogenes group encompassing Streptomyces diastatochromogenes, Streptomyces bottropensis and Streptomyces neyagawaensis (Takeuchi et al., 1996). Streptomyces acidiscabies and other pathogenic strains fall into a group with similarities to the Streptomyces albidoflavus group of Williams et al. (1983).
The taxonomy of potato-scab-causing Streptomyces spp. has been studied by many microbiologists on the bases of numerical analysis of phenotypic characteristics (Faucher et al., 1995), fatty acid and protein profile analyses (Paradis et al., 1994), DNA–DNA hybridization (Healy & Lambert, 1991; Bouchek-Mechiche et al., 2000) and 16S rRNA gene sequence analysis (Takeuchi et al., 1996; Kreuze et al., 1999). 16S rRNA gene sequencing is a powerful method for elucidating phylogenetic relationships among prokaryotic organisms (Woese, 1987; Stackebrandt et al., 1997) and has been used to facilitate the differential identification of the genus Streptomyces (Mehling et al., 1995; Kreuze et al., 1999). Nevertheless, 16S rRNA gene sequences may be insufficient to define phylogenetic relationships among closely related species and among strains belonging to a species because of the evolutionary conservation of 16S rRNA (Woese, 1987). In comparison with 16S rRNA gene sequences, sequences of 16S–23S rDNA internally transcribed spacer (ITS) regions are more variable and have been shown to be useful in inferring the phylogenetic relationships between closely related organisms (Gürtler & Stanisich, 1996). Recently, the number, size and sequences of 16S–23S ITS regions were used for discrimination of Streptomyces albidoflavus strains (Hain et al., 1997), genetic analysis of the genus Nocardioides (Yoon et al., 1998) and clarification of the relationship between members of the family Thermomonosporaceae (Zhang et al., 2001).
In this study, we determined 16S rRNA gene sequences to classify representative scab-causing Streptomyces spp. and isolates from potato scab lesions collected in Jeju, Korea, and sequenced the 16S–23S ITS region to investigate whether this is useful for the analysis of intra- and interspecific relationships between scab-causing Streptomyces spp. and isolates.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. The strains from Jeju, Korea, were isolated from scab lesions of field-grown potato tubers from different geographic locations. All strains used in this study were grown in shaking flasks containing GYM (Streptomyces medium; DSM Z Medium 65) at 28 °C. All strains were stored at -70 °C as suspensions of spores and hyphae in 15 % (v/v) glycerol.
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), with some modifications. Mycelia (1–2 ml) grown in a GYM broth shake culture were centrifuged, rinsed with TE and resuspended in 0·4 ml SET buffer (75 mM NaCl, 25 mM EDTA, 20 mM Tris, pH 7·5). Lysozyme was added to a concentration of 1 mg ml-1 and incubated at 37 °C for 0·5–1 h. Then 0·1 vols 10 % SDS and 0·5 mg Proteinase K ml-1 were added and incubated at 55 °C with occasional inversion for 2 h. One-third volume 5 M NaCl and 1 vol. chloroform were added and incubated at room temperature for 0·5 h with frequent inversion. The mixture was centrifuged at 4500 g for 15 min and the aqueous phase was transferred to a new tube using a blunt-ended pipette tip. Chromosomal DNA was precipitated by the addition of 1 vol. 2-propanol with gentle inversion. The DNA was transferred to a new tube, rinsed with 70 % ethanol, dried under vacuum and dissolved in a suitable volume (about 100 µl) of distilled water. The dissolved DNA was treated with 20 µg RNase A ml-1 at 37 °C for 1 h. Samples were extracted in the same volume of phenol/chloroform/isoamyl alcohol (25 : 24 : 1) and precipitated with 2·5 vols cold ethanol and 0·1 vols 3 M sodium acetate. The pellets were washed with 70 % ethanol, dried and dissolved in TE or distilled water.
PCR amplification, cloning and sequencing of 16S rRNA genes and 16S–23S ITS regions.
The 16S rRNA gene was amplified using primers fD1 (5'-AGAGTTTGATCCTGGCTCAG-3') and rP2 (5'-ACGGCTACCTTGTTACGACTT-3') (Weisburg et al., 1991). The primers for amplification of the DNA fragment containing the 16S–23S ITS region were designed in this study. The sequences of the oligonucleotide primers annealing to the 16S rRNA, 16S–23S ITS and 23S rRNA flanking regions were 5'-GTCAAGTCATCATGCCCCTT-3' [primer ITSL, positions 1176–1195 (Streptomyces scabiei 16S rRNA numbering; GenBank no. AB026199)] and 5'-AAACTTGGCCACAGATGCTC-3' [primer ITSR, positions 1846–1828 (Streptomyces scabiei 16S–23S ITS and 23S rRNA numbering; GenBank no. AB026199)], respectively. The 16S rRNA gene was sequenced with primers designed by Chun & Goodfellow (1995) and the 16S–23S ITS region was sequenced by a primer (16S rRNA region 3, 5'-AAGTCGTAACAAGGTA-3') designed by Weisburg et al. (1991).
Amplification of the 16S rRNA and 16S–23S ITS regions was performed in a Peltier Thermal Cycler PTC 200 (MJ Research) in a total volume of 50 µl containing 30–50 ng DNA, 100 µM each primer, 10 µM dNTP, 10x buffer (100 mM Tris/HCl, pH 8·0, 500 mM KCl, 20 mM MgCl2, 0·1 % gelatin) and 1·5 U Taq DNA polymerase (Promega). PCR was performed under the following conditions: 4 min at 94 °C, followed by 35 cycles of 1 min at 94 °C, 1 min at 58 °C, 2 min at 72 °C. Cloning and sequencing of 16S rRNA and the 16S–23S ITS region have been described previously (Song et al., 2001).
Selection of multiple alleles of the 16S–23S ITS region.
Multiple alleles were selected on the basis of RFLP with restriction enzymes HaeIII and MspI or by random alignment with sequences of 30 clones per strain.
Data analysis.
The sequences of 16S rRNA and 16S–23S ITS determined in this study were aligned using CLUSTAL W software (Thompson et al., 1994). The nucleotide similarity values were calculated from the alignment. Evolutionary distance matrices were constructed using the algorithm of Jukes & Cantor (1969) and evolutionary trees for the datasets were inferred from the neighbour-joining method (Saitou & Nei, 1987) using MEGA version 2.1 (Kumar et al., 2001). The stability of relationships was assessed by performing bootstrap analysis of neighbour-joining data based on 1,000 resamplings.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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) of representative scab-causing and related Streptomyces spp. The result of our phylogenetic analysis was consistent with previous studies by Takeuchi et al. (1996) and Kreuze et al. (1999), but slightly different from that of Bouchek-Mechiche et al. (2000) in which Streptomyces turgidiscabies was not included. Based on phylogenetic analysis (Fig. 1), cluster I, the Diastatochromogenes group, formed diverse phyletic lines, including Streptomyces scabiei, Streptomyces europaeiscabiei, Streptomyces stelliscabiei, Streptomyces ipomoeae and Streptomyces diastatochromogenes, supported by 87 % of bootstrap replicates. Three strains, DSM 40995, 40961 and 41659, and five isolates, ADA1, ASO2, DBB1, HJA3 and SSA4, were highly related to Streptomyces europaeiscabiei (genomospecies, Bouchek-Mechiche et al., 2000), and Streptomyces scabiei. Streptomyces stelliscabiei and Streptomyces ipomoeae were related to Streptomyces bottropensis and Streptomyces neyagawaensis (98·4 and 98·6 %, respectively). The Scabiei group, encompassing Streptomyces scabiei and Streptomyces europaeiscabiei, exhibited very high similarity (>99 %) and distinct sequences (CTTGTG
GTAA-G, 1435–1439) from other groups as found by Kreuze et al. (1999). Streptomyces europaeiscabiei was differentiated from Streptomyces scabiei by one nucleotide substitution (GA, 176) and therefore it is suggested that strains DSM 40995, 40961 and 41659 should be reclassified as Streptomyces europaeiscabiei. A DNA–DNA homology study and genetic characterization other than 16S rDNA analysis should be performed to confirm this opinion.
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TC (position 175–176) and GATGAGTG-GGGCGGGGG (193–200). The unique nucleotide (AG) was at position 376. The two distinct regions are positioned in a major variable region (
-region) of 16S rRNA genes (Kreuze et al., 1999). It is thought that the -region is a valid region for use in rapid identification of Streptomyces spp.
In cluster III, isolate KJO61 was similar to Streptomyces reticuliscabiei and Streptomyces turgidiscabies (99·4 and 99·6 %, respectively). Streptomyces strains DSM 41745, 41746 and 41747 were similar to Streptomyces turgidiscabies (99·5, 99·4 and 99·4 %) and Streptomyces reticuliscabiei (99·7, 99·6 and 99·7 %). This result was similar to an earlier study (Kreuze et al., 1999), but isolate KJO61 and Streptomyces reticuliscabiei (CFBP 4531) were closer to Streptomyces turgidiscabies rather than Finnish strains DSM 41745, 41746 and 41747. It is considered that KJO61, Streptomyces reticuliscabiei and the Finnish strains should be subjected to further genetic analyses (especially DNA relatedness with ATCC 700248) to pinpoint their taxonomic position.
Cluster IV formed two phyletic lines, including diverse Streptomyces spp., supported by 100 and 99 % of bootstrap replicates, respectively. One included Streptomyces griseus and Streptomyces setonii and the other included Streptomyces griseofuscus, Streptomyces albidoflavus, Streptomyces sampsonii, Streptomyces eurythermus and Streptomyces tendae. Streptomyces scabiei DSM 40611, 41005 and 41114 showed high similarity to Streptomyces griseus (99·5, 99·6 and 99·2 %, respectively) and should be classified as Streptomyces griseus. Streptomyces albidoflavus exhibited very high similarity (99·9 %) to Streptomyces sampsonii and was not differentiated by 16S rRNA gene sequence analysis as shown by Hain et al. (1997).
16S rRNA gene sequences are universally known as powerful tools to infer inter- and intrageneric relationships, but are too short to be useful in inferring the phylogenetic relationships between closely related organisms as described above.
Analysis of 16S–23S ITS region sequences
16S–23S ITS regions were used to evaluate whether they can be used in place of 16S rRNA genes to elucidate relationships among closely related Streptomyces species. All the strains produced one PCR product containing 16S–23S ITS fragments as determined by agarose electrophoresis. One to eight ITS alleles were selected from each organism. The ITS region sequences were determined for 111 clones of isolates and representative scab-causing strains of Streptomyces spp. (Table 1). No tRNA gene was found in the ITS sequences of Streptomyces spp. The lengths of ITS sequences (236–287 nt between positions 1531 and 1804 of the Streptomyces scabiei ITS region sequence; GenBank no. AB026199) were variable within strains as well as intra- and interspecies, and similarity among sequences was very different (35–100 %). The length and similarity of sequences of ITS alleles are listed in Table 1.
In the phylogenetic analysis based on these sequences, Streptomyces scabiei and Streptomyces europaeiscabiei clustered within a group. The similarities between type strains of Streptomyces scabiei (DSM 41658T) and Streptomyces europaeiscabiei (CFBP 4497T) varied from 73·0 to 78·5 %. Streptomyces europaeiscabiei was differentiated from Streptomyces scabiei by three gaps (positions 1600, 1631 and 1662) and by a unique sequence (CTTGGTAA, position 1658–1661). Streptomyces scabiei DSM 41659, 40961 and 40995 were closely related to Streptomyces europaeiscabiei, but not to other Streptomyces scabiei strains. It is therefore considered that Streptomyces scabiei DSM 41659, 40961 and 40995 should be reclassified as Streptomyces europaeiscabiei. Three clones of Streptomyces griseofuscus were scattered into various groups. The clones of Streptomyces eurythermus were also scattered into two groups. Streptomyces acidiscabies formed a phyletic line in a group, but Streptomyces griseofuscus and Streptomyces tendae were also included in this group. Streptomyces bottropensis and Streptomyces stelliscabiei showed that interspecies sequence homology (94·4–97·1 %) was higher than intrastrain sequence homology (78·8–100 %). Unlike in 16S rDNA analysis, Streptomyces bottropensis and Streptomyces stelliscabiei were not differentiated from each other. Streptomyces turgidiscabies and Streptomyces reticuliscabiei were not differentiated as shown by 16S rDNA data. Streptomyces diastatochromogenes divided into two phyletic lines and showed more similarity to other species (90·7 % homology with Streptomyces scabiei DSM 40962) than intrastrain similarity (84 %). It was also shown that Streptomyces ipomoeae is included in the Streptomyces neyagawaensis clade, and Streptomyces sampsonii and Streptomyces albidoflavus were mixed in a phyletic line as shown by 16S rDNA analysis. Streptomyces scabiei DSM 40611, 41005 and 41114 were closely related to Streptomyces griseus and Streptomyces setonii. The phylogenetic tree based on 16S–23S ITS region sequences is available as supplementary data in IJSEM Online.
Except for the differentiation of particular species, such as between type strains of Streptomyces scabiei and Streptomyces europaeiscabiei, the Streptomyces spp. used in this study formed a different phylogenetic lineage between various strains within species (intraspecies). The similarity between strains of species was lower than that between some closely related species. Although the 16S–23S ITS regions have been used as a tool for phylogenetic analysis of bacteria (Gonçalves & Rosato, 2002; Conrads et al., 2002) and a novel database for 16S–23S ITS regions has been created (García-Martínez et al., 2001), this study of intraspecific 16S–23S ITS region sequences of Streptomyces spp. has revealed that they are not useful in phylogenetic analysis. In other words, the 16S–23S ITS regions were of no use as a genetic marker to elucidate relationships among the Streptomyces spp. used in this study. In other studies (Gürtler & Stanisich, 1996; Hain et al., 1997; Gonçalves & Rosato, 2002; Conrads et al., 2002) and in this study, it is suggested that 16S–23S ITS region sequences are a powerful tool for phylogenetic analysis of Gram-negative bacteria, but not of Gram-positive bacteria, especially Streptomyces spp.
In conclusion, based on phylogenetic analysis of 16S rRNA gene sequences, most of the Streptomyces spp. isolated from potato scab lesions in this study were classified into Streptomyces scabiei and Streptomyces acidiscabies. It is thought that Korean isolate KJO61, Streptomyces reticuliscabiei and Finnish strains related to Streptomyces turgidiscabies should be analysed by other genetic methods or DNA–DNA relatedness to clarify their taxonomic position. From the data obtained in the 16S–23S ITS region sequence analysis, it was revealed that Streptomyces europaeiscabiei could be clearly differentiated from Streptomyces scabiei. However, it was confirmed that ITS regions are not useful in the phylogenetic analysis of Streptomyces spp.
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