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Division of Applied Life Science (BK 21), PMBBRC and EB-NCRC, Gyeongsang National University, Jinju 660-701, Republic of Korea
Correspondence
Young Ryun Chung
yrchung{at}gnu.ac.kr
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ABSTRACT |
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9c and C18 : 17c) supported the affiliation of strain YC5194T to the genus Lysobacter. Phylogenetic analysis based on 16S rRNA gene sequences, DNA–DNA hybridization data and biochemical and physiological characteristics strongly supported the genotypic and phenotypic differentiation of strain YC5194T from species of Lysobacter with validly published names. Strain YC5194T therefore represents a novel species, for which the name Lysobacter capsici sp. nov. is proposed. The type strain is YC5194T (=KCTC 22007T =DSM 19286T).
Transmission electron micrographs of cells of strain YC5194T, TLC of polar lipids of two related type strains, fatty acid profiles and API ZYM results for strain YC5194T and related type strains and a detailed antimicrobial spectrum for strain YC5194T are available as supplementary material with the online version of this paper.
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MAIN TEXT |
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). The initial description for the genus Lysobacter reported in the 1970s was based primarily on phenotypic characteristics; recently, the genus Lysobacter has been recognized in the phylum Proteobacteria with the help of polyphasic taxonomy (Lee et al., 2006; Weon et al., 2006; Yassin et al., 2007).
Some Lysobacter strains have been reported to have antifungal and antimicrobial activities. Lysobacter sp. XL1 produces lysoamidase, from which a drug is derived that is used in the treatment of external infections caused by pathogenic Gram-positive bacteria. It is also effective against many yeast and fungi groups (Ryazanova et al., 2005). Lysobacter enzymogenes was shown to be a potential biocontrol agent for plant fungal pathogens (Folman et al., 2004; Kilic-Ekici & Yuen, 2003). Lysobacter sp. SB-K88, previously known as a Stenotrophomonas strain (Nakayama et al., 1999), produces three antifungal compounds, xanthobaccins A, B and C; xanthobaccin A suppresses the sugar beet damping-off disease (Islam et al., 2005). Some Lysobacter isolates had strong antibiotic activity against Gram-positive bacteria, especially meticillin-resistant Staphylococcus aureus (Ahmed et al., 2003; Chohnan et al., 2002; Hashizume et al., 2001, 2004; Kato et al., 1998).
Strain YC5194T was identified on the basis of 16S rRNA gene sequences, DNA–DNA hybridization data and other chemotaxonomic and genotypic characteristics as belonging to a novel species in the genus Lysobacter.
In the process of screening biological control agents for plant-pathogenic fungi, especially those active against Pythium ultimum and Colletotrichum gloeosporioides, soil samples were collected from the rhizosphere of pepper (Capsicum annuum L.) in Jinju, Korea, in July 2003. Ten grams of each soil sample was serially diluted in 100 ml distilled deionized water. Plates containing 2 % tryptic soy agar (2 % TSA; Difco) (pH 7.2) were inoculated with 0.1 ml aliquots and incubated at 28 °C for 3 days. Only bacterial strains with antifungal or antibacterial activity were selected (Chung et al., 1999, 2000). The details of fungal, yeast and bacterial strains used to check antimicrobial activity are given in Supplementary Table S3 (available in IJSEM Online). Strain YC5194T, with a broad antifungal spectrum, was further investigated for its taxonomic position because the 16S rRNA gene sequence of the strain was most closely related to those of species of the genus Lysobacter (<94.0 to >99.0 % sequence similarity).
Cell morphology was observed under a Nikon light microscope at x1000 magnification and by using a transmission electron microscope (Hitachi H-600) with cells grown for 1 day at 28 °C on 2 % TSA. Catalase and oxidase tests were performed by the procedures outlined by Cappuccino & Sherman (2002). Carbohydrate assimilation and enzyme activities were determined by using API ID 32 E and API ID32 STREP at 30 °C and API ZYM at 37 °C according to the instructions of the manufacturer (bioMérieux). Growth at different temperatures (4, 15, 20, 28, 37 and 45 °C) was tested on 2 % TSA. Anaerobic growth was tested at 28 °C by pouring a thick layer of vaspar (50 % petrolatum, 50 % paraffin) on the surface of inoculated 2 % TSA in 35 ml screw-capped glass tubes (Costilow, 1981). Degradation of chitin, starch, gelatin and Tween 20 was investigated by using the protocols outlined by Atlas (1993). Growth at different temperatures and pH was assessed after 3 days incubation. Salt tolerance was tested in 2 % TSA broth medium supplemented with 1–10 % (w/v) NaCl after 7 days incubation. Duplicate antibiotic-sensitivity tests were done using filter-paper discs containing the following: tetracycline, kanamycin, ampicillin (Sigma) and rifampicin, each at concentrations of 10, 50 and 100 µg ml–1. Discs were placed on 2 % TSA plates that had been spread with strain YC5194T or reference strains and the plates were then incubated at 28 °C for 3 days. Almost all tests were also performed with reference strains Lysobacter gummosus KCTC 12132T, Lysobacter antibioticus KCTC 12129T, Lysobacter enzymogenes KCTC 12131T, Lysobacter koreensis KCTC 12204T, Lysobacter daejeonensis DSM 17634T and Lysobacter yangpyeongensis DSM 17635T.
Extraction of genomic DNA was done using a commercial genomic DNA extraction kit (Core Biosystem). The 16S rRNA gene of strain YC5194T was PCR-amplified from a small amount of purified genomic DNA by using primers 27F and 1492R (Lane, 1991). The PCR product obtained was purified and sequenced according to Chung et al. (1999). 16S rRNA gene sequence was compiled using SeqMan software (DNASTAR) and the sequences of related taxa were obtained from the GenBank database. Multiple alignments were performed by CLUSTAL_X (Thompson et al., 1997) and gaps were edited in the BioEdit program (Hall, 1999). Evolutionary distances were calculated using Kimura's two-parameter model (Kimura, 1983). Phylogenetic trees were constructed by using neighbour-joining (Saitou & Nei, 1987) and maximum-parsimony (Fitch, 1971) methods in the MEGA3 program (Kumar et al., 2004) with bootstrap values based on 1000 replications (Felsenstein, 1985).
For the measurement of G+C content of the chromosomal DNA, genomic DNA of strain YC5194T was extracted and purified as described by Ausubel et al. (1995). DNA was then enzymically degraded into nucleosides and the G+C content was determined as described by Mesbah et al. (1989) using reversed-phase HPLC. Cellular fatty acids were analysed using Lysobacter strains grown on TSA for 2 days at 28 °C. Cellular fatty acids were saponified, methylated and extracted according to the protocol of the Sherlock Microbial Identification System version 4.0 software (MIDI). Fatty acids analysed by GC (Hewlett Packard 6890) were identified using the Microbial Identification software package (Khan et al., 1996). The quinone system and polar lipids were determined by TLC, as described by Lechevalier et al. (1977) and Tindall (1990).
DNA–DNA hybridization was carried out to evaluate the genomic DNA relatedness between strain YC5194T and those Lysobacter strains that had high 16S rRNA gene sequence similarity (>97.0 %) to strain YC5194T (Stackebrandt & Goebel, 1994; Wayne et al., 1987). Extracted genomic DNA was fragmented with HaeIII for slot hybridization. Digested DNAs were diluted serially and loaded into slots with three replications for each sample and DNAs were used individually as labelled probes for cross-hybridization. Randomly primed DNA labelling with digoxigenin-dUTP and hybridization (hybridization temperature, 53 °C; washing temperature, 65–68 °C) were performed using a DIG High Prime DNA labelling kit (Roche Applied Science) according to the manufacturer's instructions and standard procedures (Lim et al., 2005; Sambrook & Russell, 2001). The signals of the dilution series were quantified using Bio-Rad GelDoc scanning software. The signals produced by self-hybridization were inferred as 100 %, and hybridization values (%) were calculated from the results of three experiments.
The novel strain was Gram-negative and non-motile and had gliding activity. Cells were rod-shaped (0.3–0.5x2.0–20 µm) and occurred singly and in pairs and irregular filament-like forms (Supplementary Fig. S1). Colonies grown on 2 % TSA plates for 3 days were smooth, circular and creamy white to yellow, 2–4 mm in diameter, and they changed form as they grew older due to motility. Fruiting bodies were not observed. Growth was facultatively anaerobic. Only strain YC5194T of seven tested Lysobacter strains had 
-galactosidase activity. Physiological characteristics of strain YC5194T are summarized in the species description and a comparison of selective characteristics with related type strains is shown in Table 1.
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9c (9.3 %), C18 : 17c (6.5 %), iso-C11 : 0 3-OH (3.8 %), iso-C17 : 0 (3.7 %), iso-C11 : 0 (2.3 %), C16 : 111c (2.2 %), C14 : 0 (1.9 %), C15 : 0 (1.7 %) and trace amounts (<1.0 %) of some other fatty acids were detected, which are shown in Supplementary Table S1. Although the major fatty acids were similar to those of other members of the genus Lysobacter, significant differences were found between different species in the genus and the novel strain. C9 : 0 and C16 : 111c (2.2 %) were detected only in strain YC5194T (Supplementary Table S1). The following polar lipids are present: diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol and phosphatidyl-N-methylethanolamine. An unknown polar lipid AL1 (amino group-containing lipid) was also detected (Fig. 1). The polar lipids of two closely related type strains, L. gummosus KCTC 12132T and L. antibioticus KCTC 12129T, were also determined. The major polar lipids were the same, but the unknown amino group-containing lipids differed from species to species (Fig. 1 and Supplementary Fig. S2).
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).
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). Q-8 was the major quinone in strain YC5194T and in all type strains of recognized Lysobacter species.
The 16S rRNA gene sequence of strain YC5194T was a continuous stretch of 1470 bp. Sequence similarity calculations after a neighbour-joining analysis indicated that the closest relatives of the novel strain were L. gummosus ATCC 29489T (99.59 % similarity), L. antibioticus DSM 2044T (99.40 %), L. enzymogenes DSM 2043T (97.35 %) and L. koreensis KCTC 12204T (97.0 %); low levels of similarity (<97.0 %) were found with other type strains of the genus Lysobacter. Phylogenetic trees based on the neighbour-joining and maximum-parsimony methods (Fig. 3) showed that strain YC5194T formed a cluster supported with a high bootstrap value (100 %).
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; Wayne et al., 1987). According to Fox et al. (1992) and Stackebrandt et al. (2002), 16S rRNA gene sequences, protein-coding gene sequences and DNA–DNA hybridization should be considered as molecular criteria for species delineation. In cases of very high similarity (16S rRNA gene sequences), DNA–DNA hybridization is a more powerful and helpful tool to distinguish strains at the species level.
Thus 16S rRNA gene sequence similarity, phylogenetic analysis, G+C content, Gram-staining behaviour (Gram-negative), gliding activity and other enzyme activities clearly indicate that strain YC5194T belongs to the genus Lysobacter. To the best of our knowledge, this is the first classified member of the genus Lysobacter that has antifungal activity against Pythium ultimum. Strain YC5194T also showed different results in antibiotic-sensitivity tests compared with reference strains (L. gummosus KCTC 12132T, L. antibioticus KCTC 12129T and L. enzymogenes KCTC 12131T). Strain YC5194T is positive for chitinase, gelatinase and lipase but negative for hydrolysis of starch, agar and cellulose. Thus, low DNA–DNA relatedness with other Lysobacter species, significant differences in fatty acid profiles (Supplementary Table S1), polar lipid differences (Fig. 1
and Supplementary Fig. S2), phylogenetic trees (Fig. 3), antibiotic sensitivities and some physiological and biochemical characteristics (Table 1, Supplementary Table S2 and Supplementary Fig. S2) clearly distinguish strain YC5194T as a member of a novel species of the genus Lysobacter, for which the name Lysobacter capsici sp. nov. is proposed.
Emended description of the genus Lysobacter
Characteristics are the same as given in the original description of the genus Lysobacter (Christensen & Cook, 1978) with the following amendment. The genus Lysobacter has the following polar lipids: diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol and phosphatidyl-N-methylethanolamine. Some unknown amino group-containing lipids are also present, which may differ from species to species (Fig. 1 and Supplementary Fig. S2).
Description of Lysobacter capsici sp. nov.
Lysobacter capsici (cap'si.ci. N.L. gen. n. capsici of Capsicum, referring to the isolation of the type strain from the rhizosphere of Capsicum annuum L.).
Cells are Gram-negative, facultatively anaerobic, rod-shaped, non-spore-forming and non-motile but having gliding activity, 0.3–0.5 µm wide by 2.0–20 µm long. Cells occur singly and in pairs and can form irregular filament-like structures. Colonies grown on 2 % TSA at 30 °C for 3 days are 2.0–4.0 mm in diameter, creamy white to yellow, smooth and circular. The temperature range for growth is 15–37 °C (very weak growth at 4 °C); no growth occurs at 45 °C. The optimum temperature for growth is 28 °C. The pH range for growth is pH 5.5–8.5, with an optimum of pH 7.0–7.5. Growth occurs in the absence of NaCl and in the presence of 1.0–2.0 % (w/v) NaCl, but not in 3.0 % (w/v) NaCl. Sensitive to 10 µg rifampicin, 50 µg kanamycin and 50 µg tetracycline ml–1, but resistant to 100 µg ampicillin ml–1. Catalase- and oxidase-positive. Uses 5-bromo-3-indoxyl nonanoate, 4-nitrophenyl β-D-glucopyranoside and 4-nitrophenyl β-D-galactopyranoside as sole carbon sources but not the following: L-arabitol, galacturonic acid, potassium 5-ketogluconate, sodium pyruvate, D-mannitol, maltose, adonitol, palatinose, L-tryptophan, 5-bromo-4-chloro-3-indolyl N-acetyl-β-D-glucosaminide, D-glucose, sucrose, L-arabinose, D-arabitol, trehalose, D-rhamnose, inositol, cellobiose and D-sorbitol. Acid is produced from ribose, mannitol, sorbitol, lactose, trehalose, raffinose, glycogen, pullulan, maltose, melibiose, melezitose, methyl β-D-glucopyranoside and tagatose. Urea is not hydrolysed. Cannot produce acid from sucrose, L-arabinose, D-arabitol or cyclodextrin. Tests for β-glucuronidase and β-mannosidase are positive. Acetoin is not produced. Enzyme activities for chitinase, alkaline phosphatase, esterase (C-4), esterase lipase (C-8), lipase (C-14), leucine arylamidase, trypsinase, acid phosphatase, naphthol-AS-BI-phosphohydrolase, -galactosidase, -glucosidase and β-glucosidase are present, but valine arylamidase, cystine arylamidase, -chymotrypsin, β-galactosidase, β-glucuronidase, N-acetyl-β-glucosaminidase, -mannosidase and -fucosidase activities are absent. Q-8 is the major quinone. Has the major polar lipids listed in the amended genus description. The DNA G+C content of the type strain is 65.4 mol%.
The type strain, YC5194T (=KCTC 22007T =DSM 19286T), was isolated from the rhizosphere of pepper in Jinju, Korea.
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ACKNOWLEDGEMENTS |
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