Vibrio navarrensis sp. nov., a Species from Sewage

June 13, 2017 | Autor: Patrick Grimont | Categoria: Nucleic acid hybridization, Phenotype, Vibrio, Sewage, Water Microbiology
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Vol. 41, No. 2

INTERNATIONAL JOURNAL OF SYSTEMATIC BACTERIOLOGY, Apr. 1991, p. 290-294 0020-7713/91/020290-05$02.0010 Copyright 0 1991, International Union of Microbiological Societies

Vibrio navarrensis sp. nov., a Species from Sewage MARIA C. URDACI,1-2* MICHEL MARCHAND,' ELISABETH AGERON,2 JOSE M. ARCOS,3 BEGONIA SESMA,3 AND PATRICK A. D. GRIMONT2 Laboratoire de Microbiologie, Universite' de Bordeaux I , avenue des Facultks, F-33405 Talence,' and Unite' des Entkrobactkries, Institut National de la Sante' et de la Recherche Mkdicale Unite' 199, Institut Pasteur, F-75724 Paris Cedex 15,2 France, and Instituto de Salud Publica de Navarra, Pamplona, Spain3 A group of 11 strains, mostly isolated from sewage water in the Province of Navarra, Spain, were found to constitute a DNA relatedness group which is 2 to 39% related to 23 species of the genus Vibrio and 2 to 3% related to two Aeromonas species. Phenotypically, these strains have all of the properties that define the genus Vibrio. However, they differ from the previously described species by three or more properties. The strains are negative for arginine, ornithine, and lysine decarboxylase activities and the Voges-Proskauer test and are unable to utilize putrescine, gluconate, glucuronate, and histidine. They utilize and produce acid from sucrose and grow at 40°C. All strains grow in the presence of 0.5% (wthol) NaCl, and seven strains grow weakly in peptone water lacking NaCl. The group of strains which we studied can also be differentiated from other Vibrio species by fatty acid content. The G+C ratio of the DNA is 45 to 47 mol%. The name Vibrio navarrensis sp. nov. is proposed for these strains; strain 1397-6 (= CIP 103381) is the type strain.

During a survey to determine the distribution of pathogenic Vibrio cholerae in rivers, lakes, and sewage of the province of Navarra, Spain, a group of 11 phenotypically similar bacteria were isolated. These strains could not be identified as any of the 20 Vibrio species described in Bergey's Manual of Systematic Bacteriology (2) or as any of the 11newly described Vibrio species (3, 6, 9, 13, 14, 16, 19, 21, 22, 24, 31). In this paper, we demonstrate that the strains which we studied (i) belong in the genus Vibrio, (ii) constitute a new DNA relatedness group (genomic species) in the genus Vibrio, and (iii) can be differentiated from the previously described species by phenotypic properties. The name Vibrio navarrensis is proposed for the new species. MATERIALS AND METHODS Bacterial strains. The 11 V. navarrensis strains which we studied included 6 strains isolated from sewage at Villafranca, Navarra, Spain, in July 1982 and 5 strains isolated from the following five locations in Navarra Province: Pitillas (sewage, May 1982), Peralta (sewage, June 1983), Murillo del Fruto (sewage, November 1982), Cortes (irrigation water, October 198l), and Salado River (August 1983). These strains were isolated by using standard procedures (25). The type strains used in DNA relatedness experiments are listed in Table 1. Conventional tests. The biochemical characteristics recommended for genus and species assignments were determined as previously described (30). Photomicrographs of cells negatively stained with 1%(wthol) phosphotungstic acid in water (pH 7.0) were taken at the Electron Microscopy Facility, University of Oldenburg, Oldenburg, Federal Republic of Germany. Nutritional tests. Carbon source utilization tests were performed by using specially manufactured API strips (API System, La Balme les Grottes, France) which contained pure carbon sources and were similar to API CH, API A 0 and API AA galleries (lo), except that the total number of tests was limited to 99 carbon sources (11). The minimal

* Corresponding author

medium (supplied by API System) contained 25 g of NaCl per liter, 0.2 g of MgC1, per liter, and 16 growth factors (11). A total of nine strains were tested. A 2-ml portion of a calibrated (100 Klett units, corresponding to a no. 3 standard on the MacFarland opacity scale) bacterial suspension in 2.5% NaCl in water was added to 60 ml of minimal medium. The mixture was distributed into API cupules. The strips were incubated at 30°C and examined for growth daily for 6 days. DNA-DNA hybridization. Previously described procedures were used to extract, purify, and shear unlabeled DNAs (7). The exact procedures used for in vitro labeling of DNA with tritium-labeled nucleotides and for hybridization experiments (S1 nuclease-trichloroacetic acid method) have been described previously (12). The temperature (T,) at which 50% of the reassociated DNA became hydrolyzable by S1 nuclease was determined by the method of Crosa et al. (8). The difference between the T,,, of the homoduplex (in the homologous reaction) and the T, of a heteroduplex (in a heterologous reaction) is an estimate of divergence between two DNAs (4). DNA base composition. The base compositions of the DNAs from strains 1397-6T(T = type strain) and 1383-2 were determined from the midpoint values of the thermal denaturation profiles by L. Stal, University of Oldenburg. RESULTS AND DISCUSSION

The phenotypic properties common to all of the strains from Navarra, Spain, which we studied are given in the species description below. Identification to genus level. The 11 strains from Navarra have all of the properties of the genus Vibrio. The cells are gram negative and polarly flagellated (Fig. 1). The strains are facultative anaerobes, are able to produce acid from glucose under anaerobic conditions, and are halotolerant (good growth in peptone water containing 7% [wt/vol] NaC1) and moderately halophilic (seven strains grow weakly and four do not grow in peptone water without NaCl; all grow well in the presence of 0.5% [wt/vol] NaCl). All of the strains tested failed to fix nitrogen (27). All of the strains were oxidase positive, reduced nitrate into nitrite, and were susceptible to vibriostatic compound 0 0 2 9 (2,4-diamino-6,7-diisopropyl-

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TABLE 1. Levels of DNA relatedness of strain 1397-6Tto other V . navarrensis strains, Vibrio species, and related bacteria Source(s) of unlabeled DNA“

Origin

V . navarrensis 1397-6T(=CIP 103381T) V . navarrensis 1383-1 V . navarrensis 1383-2 V . navarrensis 1397-4 V . navarrensis 1397-9 V . navarrensis 1045 V . navarrensis 1099-2 V . navarrensis 2232 V . navarrensis 2825 V . navarrensis 1381-1 V . natriegens ATCC 14048= V. proteolyticus ATCC 15338= V . damsela CIP 102761T (=NCIMB 2184, ATCC 33539) V . parahaemolyticus ATCC 17802T V . fluvialis ATCC 33809= V . vulnificus ATCC 27562T V . harveyi NCIMB 1280T (=ATCC 14126) V . orientalis CIP 102891T (=ATCC 33934) V . cincinnatiensis ATCC 35912= V . campbelii NClMB 1894T(=ATCC 25920) V . tubiashii CIP 102760T(=ATCC 19109) V . dginolyticus NCIMB 1903T(=ATCC 17749) V . pelagius CIP 102762T (=ATCC 25916) V . diazotrophicus ATCC 33466= V . nereis NCIMB 1897T (=ATCC 25917) V . cholerae NCTC 8021T (=ATCC 14035) V . mimicus ATCC 33653T V . metschnikovii ATCC 7708T V . angliillarum NCIMB 6T (=ATCC 19264) V . mediterranei CECT 621T (=ATCC 43341) V . ordaiii NCIMB 2167T (=ATCC 33509) V . costicola NCIMB 701T (=ATCC 33508) V .fischeri NCIMB 1281T(=ATCC 7744) A . hydrophila ATCC 7966= A . caviae ATCC 15468T E. coli K-12

Sewage, Villafranca, Spain Sewage, Villafranca, Spain Sewage, Villafranca, Spain Sewage, Villafranca, Spain Sewage, Villafranca, Spain Sewage, Peralta, Spain Sewage, Pitillas, Spain Sewage, Murillo del Fruto, Spain Irrigation water, Cortes, Spain Salado River, Spain

9% Relative reassociation with strain 1397-6T at 60°C

100 82 96 92 94 88 98 90 89 74 39 15 15 15 15 14 12 11 11 11 11 10 10 10 9 9 9 7 7 7 6 3 2 2 3 3

* Tm (“‘Ib 0.0 2.0 0.0 1.o 2.0 1.5 4.0

a ATCC, American Type Culture Collection, Rockville, Md. ; CECT, Coleccion Espafiola de Cultivos Tipo, Valencia, Spain; CIP, Collection de 1’Institut Pasteur, Paris, France; NCIMB, National Collections of Industrial and Marine Bacteria, Aberdeen, Scotland. A T,, Difference between the T , of the homoduplex (in the homologous reaction) and the T, of a heteroduplex (in a heterologous reaction).

pteridine). The G + C contents of the DNAs from two strains were 45 and 47 mol%. These values are in the known range for the genus Vibrio (39 to 50 mol% for the genus; 47 to 49 mol% for Vibrio cholerae and Vibrio mimicus [2]) and preclude assignment of our strains to the following genera: Aeromonas (57 to 63 mol% [20]), Allomonas (57 mol% [171), Photobacterium (39 to 44 mol% [l]),Plesiomonas (50 to 52 mol% [23]), and most genera in the family Enterobacteriaceae (50 to 60 mol% [5]). DNA relatedness. The levels of DNA relatedness of strain 1397-6T to nine other strains from Navarra, 23 Vibrio species, two Aeromonas species, and Escherichia coli are shown in Table 1. The 10 strains from Navarra constituted a tight DNA genomic species, whereas the most closestly related Vibrio species (Vibrio natriegens) was only 39% related to strain 1397-6T. Because of the known standard error associated with the hybridization method (12), the levels of DNA relatedness between strain 1397-6Tand Vibrio costicola, Vibrio Jischeri, Aeromonas hydrophila, Aeromonas caviae, and E . coli were negligible. Thus, the strains from Navarra constitute a new genomic species in the genus Vibrio. Phenotypic differentiation of the new genomic species. In a recent study of the fatty acid contents of Vibrio species (26),

FIG. 1. Transmission electron micrograph of a cell of V . navarrensis CIP 103381Twith a polar flagellum.

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TABLE 2. Characteristics useful for distinguishing Vl navarrensis from previously described Hbrio species Growth at:

Utilization of:

+ + + + + + d + + + +

V: navarrensis K natriegens K parahaemolyticus V. vulnificus Vl haweyi K cincinnatiensisb V. campbellii F/. alginolyticus I/. pelagius cholerae mimicus ordalii fischeri splendidus 11" hollisaed mediterraneie nigrapulchritudd logei marind diazotrophicush proteolyticus damsela' fluvialis orientalis' nereis anguillarum costicola splendidus I fumissiik aestuarianus' tubiashii"

-

-

+-

d

+ + + + + + + + + d + ND +

-, All strains negative; f, all strains positive; d, strains differ in their reactions; ND, no data available. The data for species other than V. navarrensis were taken from previously published work and checked in our laboratory. The characteristics given for K natriegens, V.parahaemolyticus, V.vulnificus, V. harveyi, V. campbelli, V. alginolyticus, V. pelagius, K cholerae, V. mimicus, K ordalii, K fischeri, K logei, V. proteolyticus, K JEuvialis,K nereis, K anguillarum, K costicola, and V. splendidus I are based on data from reference 2. Data from reference 3. Data from references 2, 21, and 29. Data from reference 16. Data from reference 21. Data from reference 2 and 21. g Data from references 2, 15, and 21. * Data from references 13 and 25. * Data from reference 19. Data from reference 31. Data from references 6 and 29. Data from reference 24. " Data from references 14 and 29. J

the strains from Navarra were found to be characterized by a unique fatty acid pattern. These organisms contain an unknown fatty acid that elutes just after tetradecanoic acid (26). This unknown fatty acid accounted for 1 to 3% of the total fatty acids and was not produced by other Vibrio species. In addition, C,, acids were present in larger amounts in the strains from Navarra than in other Vibrio species (26). The major characteristics that differentiate the new genomic species from the oxidase-positive species are shown in Table 2. yibrio gazogenes is oxidase and nitrate reduction negative, produces a red pigment, and is aerogenic (2,30). Vibrio

metschnikovii is also oxidase and nitrate reduction negative (2)In addition to the differential features given in Table 2, Vibrio nigrapulchritudo produces a black pigment, utilizes sorbitol and myo-inositol as sole sources of carbon and energy, and cannot grow at 37°C or in the presence of 7% (wt/vol) NaCl(2,30). Vibriohollisae is a luminous bacterium which produces acid from L-arabinose and not from maltose and cannot hydrolyze gelatin (16). Vibriofurnissii produces acid from L-arabinose and differs from our new species in its responses in many nutritional tests (6, 30). Vibrio marinus cannot grow at 37°C or in the presence of 7% (wt/vol) NaC1, cannot hydrolyze starch, and cannot produce acid from

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VZBRZO NAVARRENSZS SP. NOV.

mannitol(l5, 18, 30). Vibrio splendidus I is luminescent, and Vibrio spendidus I1 cannot grow at 37°C (2, 29, 30). Vibrio aestuarianus produces acid from lactose (24). Thus, the strains from Navarra constitute a genomic species which can be identified by phenotypic properties. On the basis of the criteria recommended by a group of experts (28), these strains constitute a new species, for which the name Vibrio navarrensis is proposed. The public health significance of V . navarrensis remains to be determined. This species was isolated at the same time as V. cholerae 01 and non-01 in sewage and contaminated river water. Further studies are needed to demonstrate any pathogenic role for V. navarrensis. Description of Vibrio navarrensis sp. nov. Vibrio navarrensis (na.var.ren’sis. L. gen. n. navarrensis, of Navarra, the Spanish province where the organism was isolated). Cells are gram-negative, nonsporeforming rods that are 1 to 2 by 0.8 to 1 bm and are motile by means of a single polar flagellum (when grown on solid media or in liquid media) (Fig. 1). Chemoorganotrophic with both oxidative and fermentative metabolism. Oxidase and catalase positive. Reduces nitrate to nitrite. No growth or weak growth when NaCl is absent from the culture medium. Colonies on nutrient agar supplemented with 2% (wthol) NaCl are 2 to 3 mm in diameter after overnight incubation at 30”C, round, opaque, and nonpigmented and do not swarm. They are not luminescent. Colonies on thiosulfate-citratebile salts-sucrose agar are yellow (sucrose positive). All strains grow in media containing 7% NaCl. No growth occurs in the presence of 10% NaCl. Growth is optimal at 30 to 37°C but also occurs at 40°C. Most strains grow at 10°C (7 of 11strains) and 42°C (9 of 11strains). Does not fix nitrogen. Indole is produced, gelatin and starch are hydrolyzed, and acid (but no gas) is produced from D-fructose, D-galactose, D-glucose, D-mannitol, maltose, and sucrose. Susceptible to 2,4-diamino-6,7-diisopropylpteridine(vibriostatic agent 0/129). H,S is not produced from glucose-lactose-iron or triple sugar iron agar; urease, tryptophanase , arginine dihydrolase (Thornley-Moeller media), and lysine and ornithine decarboxylases are not produced. Negative Voges-Proskauer reaction. Acid is not produced from L-arabinose, L-rhamnose, D-sorbitol, and lactose. Esculin is blackened by six of nine strains tested (in API assimilation strips). Hydroxyquinoline-P-glucuronide is not hydrolyzed (in API assimilation strips). The nine strains subjected to assimilation tests utilize 24 substrates and do not utilize 63 other substrates. Variable results are obtained with the following substrates (the number of strains positive is given in parentheses): D-cellobiose (eight), citrate (eight), D-malate (eight), 2-ketoglutarate (seven), cis-aconitate (seven), L-tyrosine (seven), D-turanose (five), palatinose (four), and D-galactose (three). All V. navarrensis strains utilize the following substrates as sole carbon and energy sources: N-acetylglucosamine, D-alanine, L-alanine, L-aspartate, D-fructose, fumarate, gluconate, glucosamine, D-glucose, L-glutamate, m-glycerate, glycerol, DL-lactate, L-malate, maltose, maltotriose, D-mannitol, P-methyl-D-glucoside, L-proline, D-ribose, L-serine, succinate, sucrose, and trehalose. None of the strains utilize the following substrates as sole carbon and energy sources: trans-aconitate, adonitol, DL-5aminovalerate, ~~-4-aminobutyrate, L-arabinose, D-arabitol, L-arabitol, benzoate, betaine, caprate, caprylate, mesocoumarate,dulcitol, meso-erythritol, ethanolamine, L-fucose, galacturonate, P-gentiobiose, gentisate, glucuronate, glut-

293

arate, histamine, L-histidine, 3-hydroxybenzoate, 4-hydroxybenzoate, ~~-3-hydroxybutyrate, myo-inositol, itaconate, 2-ketogluconate, 5-ketogluconate, lactose, lactulose, D-lyxose, malonate, maltitol, D-melezitose, melibiose, methyl-aD-galactoside, methyl-P-D-galactoside, 3-methyl-a-glucose, methyl-a-D-glucoside, mucate, phenylacetate, 3-phenylpropionate, propionate, protocatechuate, putrescine, quinate, raffinose, rhamnose, D-saccharate, sorbitol, L-sorbose, Dtagatose, D-tartrate, L-tartrate, meso-tartrate, tricarballylate, trigonelline, tryptamine, tryptophan, D-xylitol, and D-XYlose. Isolated from sewage and surface water. The G+C contents of the DNAs from two strains are 45 to 47 mol% (thermal denaturation method). The type strain is strain 1397-6 (= CIP 103381). Description of the type strain. Strain 1397-6T has all of the properties given above for the species. In addition, it is Simmons citrate positive, hydrolyzes o-nitrophenyl-P-D-galactopyranoside and esculin, produces acid from galactose, mannose, and glycerol, utilizes cellobiose, L-tyrosine, and 2-ketoglutarate, and grows at 10°C but not at 42°C. It grows weakly in peptone water without NaCl. The G+C content of its DNA is 45 mol%. The type strain was isolated from sewage in Villafranca, Navarra, Spain, in July 1982. ACKNOWLEDGMENTS

We thank L. J. Stal for G+C determinations. P.A.D.G. thanks R. R. Colwell for a generous gift of reference strains. REFERENCES 1. Baumann, P., and L. Baumann. 1984. Genus 11. Photobacterium Beijerinck 1889, p. 539-545. Zn N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of systematic bacteriology, vol. 1. The Williams & Wilkins Co., Baltimore. 2. Baumann, P., A. L. Furniss, and J. V. Lee. 1984. Genus I. Vibrio Pacini 1854, p. 518-550. Zn N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of systematic bacteriology, vol. 1. The Williams & Wilkins Co., Baltimore. 3. Bode, R. B., P. R. Brayton, R. R. Colwell, M. T. MacDonell, H. L. Hall, D. J. Grimes, P. A. West, and T. N. Bryant. 1986. Vibrio cincinnatiensis sp. nov., a new human pathogen. J . Clin. Microbiol. 23:104-108. 4. Brenner, D. J. 1978. Characterization and clinical identification of Enterobacteriaceae by DNA hybridization. Prog. Clin. Pathol. 7:71-117. 5 . Brenner, D. J. 1984. Family I. Enterobacteriaceae Rahn 1937, p . 408-516. I n N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of systematic bacteriology, vol. 1. The Williams & Wilkins Co., Baltimore. 6. Brenner, D. J., F. W. Hickman-Brenner, J. V. Lee, A. G. Steigerwalt, G. R. Fanning, D. G. Hollis, J. J. Farmer 111, R. E. Weaver, S. W. Joseph, and K. J. Seidler. 1983. Vibriofurnissii (formerly aerogenic biogroup of Vibriofluvialis), a new species isolated from human feces and the environment. J. Clin. Microbiol. 18:81&824. 7. Brenner, D. J., A. C. McWhorter, J. K. Leete-Knudson, and A. G. Steigerwalt. 1982. Escherichia vulneris: a new species of Enterobacteriaceae associated with human wounds. J. Clin. Microbiol. 15: 1133-1 140. 8. Crosa, J. H., D. J. Brenner, and S. Falkow. 1973. Use of a single-strand-specific nuclease for analysis of bacterial and plasmid deoxyribonucleic acid homo- and heteroduplexes. J. Bacteriol. 115:90&911. 9. Davis, B. R., G. R. Fanning, J. M. Madden, A. G. Steigerwalt, H. B. Bradford, Jr., H. L. Smith, Jr., and D. J. Brenner. 1981. Characterization of biochemically atypical Vibrio cholerae strains and designation of a new pathogenic species, Vibrio mimicus. J . Clin. Microbiol. 14:631439. 10. Gavini, F., D. Izard, H. Leclerc, M. Desmonceaux, and J. P.

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