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1 ARC Seibersdorf research GmbH, Department of Bioresources/Microbiology, A-2444 Seibersdorf, Austria
2 Laboratory of Microbiology, Universiteit Gent, Ledeganckstraat 35, B-9000 Gent, Belgium
3 Prince Edward Island Department of Agriculture and Forestry, PO Box 1600, Charlottetown, PEI, Canada C1A 7N3
4 Université de Reims Champagne-Ardenne, UFR Sciences, URVVC, Laboratoire de Stress, Défenses et Reproduction des Plantes, BP 1039, F-51687 Reims Cedex 2, France
5 Plant Research International, Wageningen, PO Box 16, 6700 AA Wageningen, The Netherlands
6 Department of Microbial Ecology, Groningen University, Biological Center, PO Box 14, 9750 RA Haren, The Netherlands
7 Institut des Sciences du Végétal, Avenue de la Terrasse, F-91198 Gif-sur-Yvette, France
8 Department of Biology, University of Waterloo, Waterloo, ON, Canada N2L 3G1
9 Department of Plant and Animal Sciences, Nova Scotia Agricultural College, PO Box 550, Truro, NS, Canada B2N 5E3
10 Department of Horticulture, Virginia Polytechnic Institute and State University, 0327-301 Saunders Hall, Blacksburg, VA 24060, USA
Correspondence
A. Sessitsch
angela.sessitsch{at}arcs.ac.at
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ABSTRACT |
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7c and summed feature 3 (comprising 16 : 17c and/or iso-15 : 0 2-OH). Isolate PsJNT showed high 1-aminocyclopropane-1-carboxylate deaminase activity and is therefore able to lower the ethylene level in a developing or stressed plant. Production of the quorum-sensing signal compound 3-hydroxy-C8-homoserine lactone was detected. Based on the results of this polyphasic taxonomic study, strain PsJNT and the seven Dutch isolates are considered to represent a single, novel species, for which the name Burkholderia phytofirmans sp. nov. is proposed. The type strain is strain PsJNT (=LMG 22146T=CCUG 49060T).
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of B. phytofirmans strains PsJNT, G44-5 and G6-5 are AY497470, AY836218 and AY836219.
A neighbour-joining tree showing the position of B. phytofirmans sp. nov. within the genus Burkholderia, a dendrogram derived from the protein patterns of the strains studied and cross-sections showing chickpea roots with strain PsJNT tagged with GFP are available as supplementary figures in IJSEM Online.
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) was originally isolated as a contaminant from Glomus vesiculiferum-infected onion roots and was subsequently shown to be a highly effective plant-beneficial bacterium (reviewed by Nowak, 1998; Nowak & Shulaev, 2003). Strain PsJNT is able to establish rhizosphere and endophytic populations associated with various plants, including potato, tomato and grapevines, where it stimulates plant growth (Frommel et al., 1991; Nowak et al., 1995; Pillay & Nowak, 1997; Bensalim et al., 1998; Ait Barka et al., 2000, 2002; Compant et al., 2005) and induces developmental changes leading to better water management (Nowak et al., 1995; Lazarovits & Nowak, 1997). Plants inoculated with strain PsJNT have been reported to produce much larger root systems, with enhanced secondary roots and more root hairs, more and larger leaf hairs, sturdier stems, and greater lignin deposits around the vascular system (Nowak, 1998). Furthermore, plants inoculated with strain PsJNT were found to contain larger amounts of phenolics and chlorophyll (Nowak et al., 1997), as well as increased levels of cytokinins (Lazarovits & Nowak, 1997) and enhanced activity of phenylalanine ammonia lyase (Nowak et al., 1997). Strain PsJNT is also able to enhance resistance to low levels of potato pathogens (Nowak et al., 1995) and tomato pathogens (Sharma & Nowak, 1998) as well as to reduce in vitro infection of grapevine by Botrytis cinerea (Ait Barka et al., 2000, 2002). Recently, during a field experiment performed in The Netherlands, seven strains with high 16S rRNA gene sequence similarity to strain PsJNT were isolated (RG31-12, RG47-8, RG47-15, G44-5, G6-5, RG44-4, RG6-12), mainly from the bulk and rhizosphere soil of maize and grass plants growing in an old grassland field (>50 years) (J. F. Salles and others, unpublished results). Additionally, in vitro dual-culture assays performed with the Dutch strains revealed that some were antagonistic to the potato pathogen Rhizoctonia solani AG-3 (Salles et al., 2005).
Based on various biochemical and physiological tests, strain PsJNT was originally classified as representing a non-fluorescent Pseudomonas sp. (Frommel et al., 1991). However, subsequent studies revealed that it represents a member of the genus Burkholderia. Phylogenetically, the genus Burkholderia belongs to the 
-Proteobacteria and currently comprises more than 30 species (Coenye & Vandamme, 2003). There are several Burkholderia species known to interact with plants. Burkholderia cepacia, the type species of the genus, was initially described as the causative agent of onion soft rot (Burkholder, 1950), but many strains belonging to the B. cepacia complex are also able to promote plant health (Parke & Gurian-Sherman, 2001). Similarly, other Burkholderia species have been reported to exhibit plant-growth-promoting or biocontrol effects (El Banna & Winkelmann, 1998; Tran Van et al., 2000; Estrada de los Santos et al., 2001).
Sequencing of the 16S rRNA gene was performed as described by Reiter et al. (2002) using the primers 8f (5'-AGAGTTTGATCCTGGCTCAG-3'), 1520r (5'-AAGGAGGTGATCCAGCCGCA-3') and 926r (5-CCGTCAATTCCTTT(AG)AGTTT-3'). Sequence assembly was performed by using the program SEQUENCHER 4.0 (Gene Codes Corporation). Phylogenetic analysis was performed with the software package ARB (Strunk et al., 2000). Multiple alignment was performed with the MULTALIN tool (Corpet, 1988) and a neighbour-joining tree based on 1298 nt was constructed using the TREECON software (Van de Peer & De Wachter, 1994) (Supplementary Fig. A in IJSEM Online). The levels of similarity between strain PsJNT and the Dutch strains were 98·8 % (strain G44-5) and 99·2 % (strain G6-5). According to 16S rRNA gene sequence analysis, strain PsJNT was closely related to Burkholderia fungorum LMG 16225T and Burkholderia caledonica LMG 19076T (both 98·6 %). 16S rRNA gene sequence similarity to Burkholderia phenazinium LMG 2247T and to Burkholderia terricola LMG 20594T was 98 %. Similarity values of 97·8, 97·5 and 97·4 % were found to the 16S rRNA gene sequences of Burkholderia graminis C4D1MT, Burkholderia xenovorans LMG 21463T and Burkholderia phymatum LMG 21445T, respectively. Similarity levels to other Burkholderia species were below 97 %, and similarity levels to other genera belonging to the -Proteobacteria were below 95·8 %.
Whole-cell protein profiles of strain PsJNT and the seven Dutch strains were determined by SDS-PAGE (Coenye et al., 2001a) and compared with over 6000 profiles in a database comprising all recognized Burkholderia, Ralstonia and Pandoraea species (Coenye et al., 2001b, 2002). Computer-assisted numerical analysis and visual comparison of the whole-cell protein profiles of strain PsJNT and the seven Dutch strains revealed that they were identical to each other and were clearly different from those of the recognized Burkholderia, Ralstonia and Pandoraea reference species (Supplementary Fig. B). Determination of the cellular fatty acid profile was determined by GLC, using the Sherlock Microbial Identification System (MIDI Inc.; database TSBA40) according to a standard protocol (Paisley, 1996). Briefly, the procedure involved saponification of whole cells in methanolic NaOH, esterification of fatty acids in acidic methanol and extraction of fatty acid methyl esters with methyl-tert-butyl ether/hexane. Strain PsJNT showed qualitative and quantitative differences in its fatty acid composition compared with closely related species. Predominant fatty acids were 16 : 0, 18 : 17c and summed features 2 and 3 (Table 1). A higher 18 : 17c content was found in strain PsJNT compared with other Burkolderia species, whereas strain PsJNT produced lower levels of 14 : 0, cyclo 17 : 0 and cyclo 19 : 08c fatty acids. In addition to these differences, strain PsJNT showed different levels of 16 : 0 3-OH, and summed features 2 and 3 compared with B. fungorum and B. caledonica (Table 1).
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) incubated at 30 °C (method outlined in Nowak & Shulaev, 2003), and forms beige-coloured colonies on 1 : 10 strength trypticase soy agar (Becton–Dickinson) at 30 °C but not at 37 °C. Classical phenotypic tests were performed with strain PsJNT and all Dutch strains as described by Vandamme et al. (1993) and Coenye et al. (2001a). API ZYM, API20 NE, ONPG and PNPG tests were performed according to the recommendations of the manufacturer (bioMérieux). Results of the phenotypic analyses are shown in Table 2 and in the species description. Strain PsJNT and the seven Dutch strains could be distinguished from closely related Burkholderia species such as B. fungorum and B. caledonica on the basis of additional biochemical properties, including growth in 10 % lactose, no growth at 37 °C, no nitrate reduction and oxidase activity (Table 2).
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. Based on 16S rRNA gene sequence data, protein profiles and biochemical data, B. fungorum, B. terricola, Burkholderia caribensis and B. xenovorans were selected as reference strains for DNA–DNA hybridization experiments. Strain PsJNT and strain R23375 (one of the Dutch isolates) showed a high DNA–DNA hybridization value (90 %). In contrast, strain PsJNT showed relatively low DNA–DNA hybridization values towards B. fungorum LMG 16225T (27 %), B. terricola LMG 20594T (21 %), B. caribensis LMG 18531T (17 %), B. graminis LMG 18924T (11 %), B. caledonica LMG 19076T (36 %) and B. xenovorans LMG 21463T (9 %).
The G+C content of the DNA was determined as described by Coenye et al. (2001a). Strains PsJNT and R23375 had G+C contents of 61·0 and 62·1 mol%, respectively, matching well with values for closely related species.
In order to show the endophytic colonization potential of strain PsJNT, a green fluorescent protein (GFP)-tagged derivative was applied for visualization of the strain on chickpea (Cicer arietinum L.) plants. Plants were inoculated with cells of the GFP-tagged PsJNT strain [107 c.f.u. (g vermiculite)–1] as described by Ait Barka et al. (2000). Plants were harvested at different times after sowing. Aggregations of GFP-expressing bacterial cells were visualized by using an Olympus fluorescence stereomicroscope (model BH2) equipped with a double set of fluorescence filters. The filter sets consisted of a 450–490 nm band-pass excitation filter and a 520 nm suppressor filter. Microscopic analyses were performed on live intact plant tissue. Just 1 day after incubation, the rhizoplane was densely colonized by strain PsJNT. More GFP-expressing cells were found on lateral roots than on the main root, and root cracks resulting from lateral root emergence were densely colonized. Four days after inoculation, PsJNT cells were found in association with root epidermal cells, parenchyma cells (Supplementary Fig. C) and xylem vessels (Supplementary Fig. D). After 6 days, PsJNT also colonized stems and leaves endophytically. In addition to chickpea endophytic colonization, the potential of strain PsJNT was also shown with potato (Frommel et al., 1991), tomato (Pillay & Nowak, 1997) and grapevines (Ait Barka et al., 2002).
Activity of the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase was determined according to Penrose & Glick (2003). ACC deaminase, commonly found in plant-growth-promoting rhizobacteria (e.g. Shah et al., 1998), cleaves the plant ethylene ACC, thereby lowering the ethylene level in a developing or stressed plant. Strain PsJNT had high ACC deaminase activity; it was able to cleave 308 nmol 
-ketobutyrate (mg protein)–1 min–1. It has been reported that 
20 nmol -ketobutyrate (mg protein)–1 min–1 is sufficient to show plant-growth-promoting effects (Penrose & Glick, 2003).
Many bacteria have evolved mechanisms to allow gene expression only when cell density is appropriate. This phenomenon is known as quorum sensing (for reviews see, for example, Whitehead et al., 2001; Fuqua & Greenberg, 2002), which, in Gram-negative bacteria, is mediated by N-acyl-homoserine lactones (NAHLs). These low-molecular-mass compounds diffuse in and out of bacterial cells and control important biological functions such as pathogenicity or plant-growth-promoting functions (Pierson et al., 1998). The production of NAHLs is common among B. cepacia strains (Gotschlich et al., 2001) and was found to control the synthesis of protease and siderophores (Lutter et al., 2001; Lewenza et al., 1999). NAHL production by strain PsJNT was determined here by TLC as described by Shaw et al. (1997). PsJNT extracts and pure NAHL were visualized with the biosensors Chromobacterium violaceum CV026 (McClean et al., 1997) and Agrobacterium tumefaciens NTLR4 (Cha et al., 1998). Results indicated the production of 3-hydroxy-C8-homoserine lactone in strain PsJNT.
Description of Burkholderia phytofirmans sp. nov.
Burkholderia phytofirmans (phy.to.fir'mans. Gr. n. phyton plant; L. part. adj. firmans strengthening; N.L. part. adj. phytofirmans plant-strengthening).
Cells are Gram-negative, non-sporulating, straight rods, 0·5–0·8 µm wide and 0·8–1·8 µm long, and are motile by a single polar flagellum (Frommel et al., 1991). Growth is observed at 30 °C but not at 37 °C. Nitrate and nitrite are not reduced. Able to assimilate D-fructose, D-xylose and D-glucose but not adonitol. Growth occurs in the presence of 0·5 % NaCl and 10 % lactose. Additional characteristics are listed in Table 2
. The following fatty acids are present in significant amounts (above 1 %): 14 : 0, 16 : 0, cyclo 17 : 0, 16 : 1 2-OH, 16 : 0 2-OH, 16 : 0 3-OH, 18 : 17c, 18 : 0, cyclo 19 : 08c, 18 : 1 2-OH, summed feature 2 (comprising 14 : 0 3-OH, iso-16 : 1 I, an unidentified fatty acid with an equivalent chain-length value of 10·928 and/or 12 : 0 ALDE) and summed feature 3 (comprising 16 : 17c and/or iso-15 : 0 2-OH). The G+C content is 61·0–62·1 mol%.
The type strain, PsJNT (=LMG 22146T=CCUG 49060T), was isolated from surface-sterilized onion roots at the Nova Scotia Agricultural College, Truro, NS, Canada (Nowak et al., 1997). Other strains (LMG 22849–LMG 22855) were isolated from the rhizosphere of maize and grasses and from the bulk soil of a Dutch field. The properties of the type strain are the same as described above for the species. In addition, the type strain will grow on cetrimide and in the presence of 1·5 and 3·0 % NaCl, will not grow in OF medium with maltose or in the presence of 4·5 % NaCl and does not show acetamide deamidase activity. The G+C content of the type strain is 61·0 mol%.
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ACKNOWLEDGEMENTS |
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