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Evaluation of the Genus Listonella and Reassignment of Listonella Damsela (Love Et Al.) Macdonell and Colwell to the Genus Photo

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Evaluation of the Genus Listonella and Reassignment of Listonella Damsela (Love Et Al.) Macdonell and Colwell to the Genus Photo INTERNATIONAL JOURNAL OF SYSTEMATICBACTERIOLOGY, Oct. 1991, p. 529-534 Vol. 41, No. 4 0020-7713/91/040529-06$02.OO/O Copyright 0 1991, International Union of Microbiological Societies Evaluation of the Genus Listonella and Reassignment of Listonella damsela (Love et al.) MacDonell and Colwell to the Genus Photobacterium as Photobacterium damsela comb. nov. with an Emended Description S. K. SMITH,l* D. C. SUTTON,l J. A. FUERST,' AND J. L. REICHELT' Sir George Fisher Centre for Tropical Marine Studies, James Cook University of North Queensland, Townsville, Queensland 481 I ,' and Department of Microbiology, University of Queetzsland, St. Lucia, Queensland 4067,2 Australia The genus Listonella, which was recently described on the basis of 5s rRNA sequence data, was found to be of dubious value on the basis of the results of a comparison of a number of taxonomic studies involving members of the Vibrionaceae. The available data suggest that 5s rRNA sequences may be of limited taxonomic use at the intra- and intergeneric levels, at least for apparently recently evolved groups, such as the Vibrionaceae. In this light, we assessed the generic assignment of the species Listonella damsela. Phenotypic characterization of 12 strains of bacteria assigned to L. damsela, including type strain ATCC 33539, revealed a strong resemblance to members of the genus Photobacterium. All of the strains conformed to major characteristics common to all known Photobacterium species. The characteristics of these organisms included the absence of a flagellar sheath and accumulation of poly-P-hydroxybutyrateduring growth on glucose coupled with the inability to utilize DL-P-hydroxybutyrate as a sole carbon source. On the basis of the phenotypic data, we propose that L. damsela should be reassigned to the genus Photobacterium as Photobacterium damsela comb. nov. ~- ._ Listonella damsela, which was initially described as present an extended description of L. damsela, which in- Vibrio damsela, is recognized as an opportunistic pathogen cludes evidence suggesting that the species should be reas- that is capable of causing disease in a variety of hosts, signed to the genus Photobacterium. This description was including damselfish (22), sharks (18), dolphins (17), and based on phenotypic data, which were analyzed in light of all humans (26). The soft tissue infection which most often currently available information (phenetic and genetic) on the occurs may be due to the production of a cytolysin (20). positions of the genera of the family Vibrionaceae. Despite recognition of the potential pathogenicity of this species, previously published taxonomic data on L. damselu are scattered and incomplete. Aside from the initial pheno- MATERIALS AND METHODS typic description (22), information useful in characterization Bacterial strains and bacteriological media. has generally been presented only in conjunction with re- The bacterial ports of disease incidence (14, 18). As a result, the generic strains used in this study and their sources are listed in Table position of L. damsela has not been adequately assessed. 1. The bacterial strains were maintained on luminous me- The current validly published generic designation of this dium (LM) at 25°C. species is the new genus Listonella (23). Establishment of The artificial seawater which we used was a modification this genus was one of a number of taxonomic changes of that described by MacLeod (25) and contained per liter of distilled water 17.55 g of NaC1, 0.75 g of KC1, 0.285 g of proposed for the family Vibrionaceae that were based on a . review of phylogenetic relationships within the family in Na,SO,, 5.10 g of MgCI, 6H,O, and 0.145 g of CaCI,. which 5s rRNA sequence data were used (23). The species The basal medium which we used was the basal medium (8), Listonella anguillarum and Listonella pelagia were also described by Baumann et al. except that it was modified described as members of this new genus, and subsequently with a lower concentration of Tris HCI (20 mM) and con- tained ferric ammonium citrate (0.025 g/liter) in place of workers have suggested that the genus Listonella may be extended to include the species currently designated Vibrio FeSO, - 7H,O. Yeast extract broth and LM were prepared tubiashii, Vibrio ordalii, Vibrio aestuarianus as described by Baumann et al. (8). and (30, 31). Phenotypic characterization. Our consideration of the generic position of L. damsela led The majority of the methods us to examine the new genus Listonella and also the appro- used in this study were methods described by Stanier et al. (8). priateness of 5s rRNA data for establishing phylogenetic (36), modified for heterotrophic marine bacteria Only significant modifications of these methods and methods from relationships within and between genera of the Vibrion- aceae. other sources are described below. Strains were incubated at In this study we took a polyphasic approach and compared 25°C for all of the tests unless otherwise stated. the relationships within the Vibrionaceae derived from 5s Cell shape, motility, and Gram stain reaction were deter- mined by using 24-h yeast extract broth cultures as previ- rRNA sequence data (with particular reference to the genus ously described Listonella) with the relationships determined by other meth- (8). ods in previous taxonomic studies. In this paper we also Flagellum characteristics were determined by using cells grown on LM for 24 h. The cells were negatively stained with membrane-filtered 1% uranyl acetate containing 0.4% sucrose, in a manner similar to that used by Allen and * Corresponding author. Baumann (l),and were examined with a Hitachi model 5 29 530 SMITH ET AL. INT. J. SYST.BACTERIOL. TABLE 1. Strains of L. darnsela used in this study described by Reichelt and Baumann (32) and was assessed by examining cells for PHB by phase-contrast microscopy. Strain Source" Isolated from: Fermentation of glucose and production of acid and/or gas 2588-80T (= ATCC 33539T) ATCC Fish ulcer were determined by using the F1 medium of Baumann et al. 0183-79 (= ACMM 625) SPHTM Human puncture wound (S), modified with a lower concentration of Tris HCI (20 mM) PD9 (= ACMM 624) SPHTM Diseased shark and the addition of bromcresol purple (0.001%). The growth PDlO (= ACMM 623) SPHTM Diseased shark 86.665H (= ACMM 620) DOAT Diseased turtle of strains in the absence of sodium ions was tested in the 86.665NH (= ACMM 621) DOAT Diseased turtle media described by Baumann and Baumann (5). Oxidase BKG/B (= ACMM 630) TVS Diseased fish reactions were tested with tetramethyl-p-phenylenediamine YC3 (= ACMM 627) ACMM Diseased fish dihydrochloride by using the technique of Stanier et al. (36). 14 (= ACMM 626) ACMM Aquarium seawater The Voges-Proskauer test was performed as described by 17 (= ACMM 632) ACMM Aquarium seawater Lee et al. (21). The ability of strains to convert arginine to PT3 (= ACMM 628) ACMM Aquarium seawater ornithine anaerobically was tested in modified Thornley FLAd (= ACMM 622) ACMM Fish surface arginine dihydrolase medium as described by Baumann and a ATCC, American Type Culture Collection, Rockville, Md.; SPHTM, P. Baumann (5). Production of the extracellular enzymes gelat- Desmarchelier, School of Public Health and Tropical Medicine, Sydney, New inase, amylase, lipase, and alginase was determined by using South Wales, Australia; DOAT, J. Carson, Department of Agriculture, Tasmania, Australia; TVS, J. Glazebrook, School of Tropical Veterinarian the methods of Baumann et al. (8). Urease activity was Science, James Cook University, Townsville, Queensland, Australia; tested in the medium of Christensen (13). Utilization of 51 ACMM, Australian Collection of Marine Microorganisms, James Cook Uni- organic carbon compounds (Table 2) as sole sources of versity, Townsville, Queensland, Australia. carbon and energy was tested as described by Baumann et al. (8). The minimal medium base used was prepared both with and without 0.05% yeast extract as a source of growth H-800 transmission electron microscope operated at an factors. The compounds tested were selected from the 150 accelerating voltage of 100 kV. compounds used by Baumann et al. (S), which were utilized The ability to accumulate poly-f3-hydroxybutyrate (PHB) by 1 to 90% of the strains examined in that study. Com- as an intracellular reserve product was tested in the media pounds that were utilized by all or no strains were not TABLE 2. Numbers of L. darnsela strains that utilize various organic compounds as sole or principal sources of carbon and energy in the presence and in the absence of 0.05% yeast extract and numbers of Photobacterium strains that utilize the compounds in the presence of 0.05% yeast extractu L. darnsela (n = 12)6 No. of strains positive Presence of Compound 0.05% yeast NO. of P. angusturn P. phosphorertm P. leiogrzuthi extract strains Atypical strain(s)' (n = 51d (n = 74)' (n = 28)' positive Cellobiose 12 0 0 0 1 ACMM 623 D-Galactose 12 5 73 28 8 ACMM 620, ACMM 621, ACMM 625, ACMM 632 D-Gluconate 0 5 63 28 0 D-Mannose 12 5 74 28 9 ACMM 620, ACMM 623, ACMM 632 Xylose 0 4 0 0 0 DL-Glycerate 12 0 68 21 0 m-Lactate 12 5 13 28 2 ATCC 33539T, ACMM 622 a-Ke tog lutarate 1 ATCC 33539T 0 0 1 0 Pyruvate 12 5 0 27 2 ATCC 33539=. ACMM 630 L-Glutamate 12 0 28 19 2 ATCC 33539=, ACMM 627 L-Serine 9 ACMM 620, ACMM 622, ACMM 625 5 26 21 0 Caprate 0 0 0 12 0 The following compounds were not utilized by any of the L. danlsela strains examined or by Photobacterium species: L-arabinose, L-rhamnose, salicin, caproate, butyrate, caprylate, heptanoate, isobutyrate, isovalerate, pelargonate, propionate, valerate, DL-P-hydroxybutyrate, aconitate, citrate, betaine, hippurate, sarcosine, glutarate, malonate, mannitol, sorbitol, ethanol, n-propanol, benzoate, p-hydroxybenzoate, quinate, tyrosine, D-a-alanine, p-alanine, y-aminobutyrate, 6-aminovalerate, arginine, citrulline, glycine, L-leucine, L-ornithine, putrescine, and spermine.
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