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Panagopoulos 1969 to a New Genus, Xylophilus Gen INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Oct. 1987, p. 422430 Vol. 37, No. 4 0020-7713/87/040422-09$02.00/0 Copyright 0 1987, International Union of Microbiological Societies Transfer of Xanthomonas ampelina Panagopoulos 1969 to a New Genus, Xylophilus gen. nov., as Xylophilus ampelinus (Panagopoulos 1969) comb. nov. A. WILLEMS, M. GILLIS, K. KERSTERS, L. VAN DEN BROECKE, AND J. DE LEY* Laboratorium voor Microbiologie en Microbiele Genetica, Rijksuniversiteit, B-9000 Ghent, Belgium Thirty-four strains of Xanthomonas ampelina, the causal agent of bacterial necrosis of grape vines, were examined by sodium dodecyl sulfate-polyacrylamide gel electrophoresis of their cellular proteins and by numerical analysis of 106 enzymatic features (API systems). These organisms formed a very homogeneous taxon. Generic and suprageneric relationships were determined by hybridizations between 23s 14C-labeled ribosomal ribonucleic acid from Xanthomonas ampelina NCPPB 2217T (T = type strain) and deoxyribonucleic acids from eight Xanthomonas ampelina strains, Xanthomonas campestris NCPPB 52€lT, and the type strains of 16 possibly related species. Xanthomonas ampelina was found to be a totally separate subbranch in ribosomal ribonucleic acid superfamily 111, without any relatives at the generic level. It is not related to the genus Xanthomonas. Genetically its closest relatives are, among others, Pseudomonas acidovorans, Alcaligenes paradoxus, and Comamonas terrigena. We propose the transfer of Xanthomonas ampelina to a new genus, Xylophilus. The only species and thus the type species is Xylophilus ampelinus. The type strain is NCPPB 2217. The causal agent of bacterial necrosis and canker of grape to a new genus, Xylophilus, as Xylophilus ampelinus (Pan- vines in the Mediterranean region and South Africa was agopoulos 1969) comb. nov. Strain NCPPB 2217 is main- originally described as Xanthomonas ampelina (16, 26). This tained as the type strain. In the rest of this paper we use the organism possesses the following features of the genus name Xylophilus ampelinus for this organism. Xanthomonas. It is an aerobic, nonsporeforming, gram-nega- tive, rod-shaped organism with one polar flagellum; it has oxidative carbohydrate metabolism; it produces a yellow MATERIALS AND METHODS insoluble pigment; and it has a mean deoxyribonucleic acid Bacterial strains. The strains which we used are listed in (DNA) base composition similar to that of the genus Table 1. They were checked for purity by plating and by Xanthomonas. However, other data clearly prove that it examination of living and gram-stained cells. In all experi- does not belong to the genus Xanthomonas. Hybridizations ments Xanthomonas and Xylophilus strains were grown on between ribosomal ribonucleic acid (rRNA) from Xantho- GYCA medium (1% [wt/vol] glucose, 0.5% [wt/vol] yeast monas campestris NCPPB 52gT (T = type strain) and DNAs extract, 3% [wthol] CaC03, 2% [wt/vol] agar); Rhodocyclus from different Xanthomonas species showed that Xantho- gelatinosus was grown on DSM medium 27 (4), and nutrient monas ampelina is definitely not related to the authentic agar (0.1% beef extract, 0.2% yeast extract, 0.5% NaC1, Xanthomonas species (11). This conclusion is supported by 0.5% peptone, 2% agar, pH 7.4) was used for all other research on the regulation of the biosynthesis of aromatic strains. All strains were grown at 28"C, except the amino acids in Pseudomonas strains and related organisms Xylophilus strains, which were grown at 24°C. In some (3, 32, 33). Additional features differentiating Xanthomonas cultures of Xylophilus ampelinus we isolated two colony ampelina from the other Xanthomonas species are the types, tl and t2, which showed similar colony morphology absence of xanthomonadins (30), very slow growth, a max- but differed in growth rate. The average colony diameters imum growth temperature of 30"C, the presence of urease, after 2 weeks on GYCA medium were 1.4 k 0.6 mm for tl utilization of meso-tartrate, and no production of acid from and 0.7 k 0.3 mm for t2. glucose or sucrose (2, 26). It is now well accepted that Enzymatic features. A total of 31 Xylophilus ampelinus Xanthomonas ampelina is not a Xanthomonas species; strains and a number of reference strains (Table 1) were however, despite its unknown taxonomic position, it has tested at 30°C in the commercially available API ZYM been maintained up to now as a separate species in this gallery and the experimental API galleries Osidases, genus (2). Esterases, and Aminopeptidases AP1, AP2, AP3, AP4, AP5, In this paper we present the results of extensive research and AP6 (API Systems S.A., La Balme-les-Grottes, on (i) the internal taxonomic structure of Xanthomonas Montalieu-Vercieu, France). The experimental procedure ampelina and (ii) its generic and suprageneric relationships. and the scoring of the results have been described previously We examined 34 strains from various geographic origins, (24). In total, 106 enzyme activities were recorded per strain. together with a number of possibly related strains and some Canberra metric coefficients (dcANB) were calculated (22) authentic Xanthomonas strains, by means of protein elec- and transformed into similarity coefficients (%S) by using the trophoresis, numerical analysis of enzymatic features, and following equation: %S = 100 x (1 - dCANB). Cluster DNA-DNA and DNA-rRNA hybridizations. Based on our analysis by the unweighted average pair group method (29) results, we propose the transfer of Xanthomonas ampelina was performed by using the Clustan 2.1 program of Wishart (34) and the Siemens model 7551 (BS2000) computer of the * Corresponding author. Centraal Digitaal Rekencentrum, Rijksuniversiteit, Ghent, 422 VOL. 37, 1987 XYLOPHILUS AMPELINUS 423 TABLE 1. Organisms used, their origins, and the tests in which they were used Species Strain" Source, place, and year of isolation Tests" Xylophilus ampelinus NCPPB 2217T (= LMG 5856T = PDDCC Vitis vinifera var. sultana, Crete, 1966 4298T = ATCC 33914T = CNBP 1192T) Xylophilus ampelinus CNBP 1192T (= LMG 5949T) Vitis viniferu var. sultana, Crete, 1966 Xylophilus ampelinus Ride AA2 (= LMG 500 = CNBP 1800) Vitis viniferu, Aude, France, 1976 Xylophilus ampelinus CNBP 1802 (= LMG 501 = Ride A1.03) Vitis vinifera, France, 1968 Xylophilus ampelinus Ride AC1 (= LMG 502 = CNBP 1803) Vitis vinifera, Aude, France, 1976 Xylophilus ampelinus CNBP 1833t1 and CNBP 1833t2 (= LMG Vitis vinifera, France, 1975 503 = Rid6 A14)" Xylophilus ampelinus CNBP 1834 (= LMG 504 = Ride A7) Vitis vinifera, France, 1975 Xylophilus ampelinus CNBP 1837t1 and CNBP 1837t2 (= LMG Vitis vinifera, France, 1975 505 = Ride C12)" Xylophilus ampelinus Ride AR1 (= LMG 506 = CNBP 1841) Vitis vinifera var. ugniblanc, Ardeche, France, 1977 Xylophilus ampelinus CNBP 1926t1 and CNBP 1926t2 (= LMG Vitis vinifera, Spain 507)' Xy lop hilus amp elin us CNBP 1927t1 and CNBP 1927t2 (= LMG Vitis vinifera, Spain 508)' Xylophilus ampelinus CNBP 1928 (= LMG 509) Vitis vinifera, Spain Xylophilus ampelinus CNBP 1938t1 and CNBP 1938t2 (= LMG Vitis vinifera, Spain 510)' Xylophilus ampelinus CNBP 2059 (= LMG 511) Vitis vinifera Xylophilus ampelinus CNBP 2060tl and CNBP 2060t2 (= LMG Vitis viniferu 512)' Xylophilus ampelinus CNBP 2061 (= LMG 513) Vitis vinifera Xylophilus ampelinus CNBP 2098 (= LMG 514) Vitis vinifera Xylophilus ampelinus NCPPB 2218 (= LMG 516 = ATCC 29074) Vitis vinifera, Greece, 1966 Xylophilus ampelinus NCPPB 2219 (= LMG 517 = ATCC 29075) Vitis vinifera, Greece, 1966 Xylophilus ampelinus NCPPB 2220 (= LMG 518 = PDDCC 4299) Vitis vinifera cv. sultana, Crete, 1966 Xylophilus ampelinus NCPPB 2221t1 and NCPPB 2221t2 (= LMG Vitis vinifera cv. sultana, Crete, 1966 519 = PDDCC 4300)' Xylophilus ampelinus NCPPB 2590 (= LMG 520) Vitis vinifera, South Africa, 1972 Xylophilus ampelinus NCPPB 2591t1 and NCPPB 2591t2 (= LMG Vitis vinifera, South Africa, 1972 521)" Xylophilus ampelinus PDDCC 4299 (= LMG 522 = NCPPB 2220) Vitis vinifera cv. sultana, Crete, 1966 Xylophilus ampelinus PDDCC 4300tl and PDDCC 4300t2 (= LMG Vitis vinifera cv. sultanu, Crete, 1969 523 = NCPPB 2221)' Xylophilus ampelinus RidC C2' (= LMG 524 = CNBP 1796) Vitis vinifera var. ugni, Charente Maritime, France, 1975 Xylophilus ampelinus RidC C13 (= LMG 525) Vitis vinifera var. ugni, Charente Maritime, France, 1975 Xylophilus ampelinus RidC 011 (= LMG 526)d Vitis vinifera var. ugni, Ile d'OlCron, France, 1969 Xylophilus ampelinus Ride 012 (= LMG 527)" Vitis vinifera var. ugni, Ile d'OlCron, France, 1969 Xylophilus ampelinus Ride P5 ( = LMG 528) Vitis vinifera var. grenache, Pyrenees Orientales, France, 1975 Xylophilus ampelinus Ride P6 (= LMG 529) Vitis vinifera, var. grenache, Pyrenees Orientales, France, 1975 Xylophilus ampelinus Ride P7 (= LMG 530 = CNBP 1799) Vitis vinifera var. macabeu, PyrCnCes Orientales, France, 1975 Xylophilus ampelinus CNBP 1800 (= LMG 544 = Ride AA2) Vitis vinifera, Aude, France, 1976 Xylophilus ampelinus CNBP 1841 (= LMG 545 = Rid6 AR1) Vitis vinifera var. ugniblunc, Ardkche, France, 1977 Xanthomonas campestris pv. NCPPB 528T (= LMG 568T = ATCC Brassica olerucea cv. gemmiferu, England, campestris 33913T) 1957 Xanthomonas campestris pv. NCPPB 1149 (= LMG 939)< Vitis carnosu, India vitiscarnosae Xanthomonas campestris pv. NCPPB 2475 (= LMG 965)' Vitis vinifera, India, 1969 viticola Xanthomonas campestris pv. NCPPB 1451 (= LMG 940)'' Vitis trifolium, India, 1961 vitistrifoliae Xanthomonas campestris pv. NCPPB 1014 (= LMG 954)' Vitis woodrowii. India vitis woodrow ii Xanthomonas albilineans NCPPB 2969T (=
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