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Beneckea PAUL BAUMANN, LINDA BAUMANN, and M

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Beneckea PAUL BAUMANN, LINDA BAUMANN, and M JOURNAL OF BACTERIOLOGY, JUly 1971, P. 268-294 Vol. 107, No. 1 Copyright 0 1971 American Society for Microbiology Printed in U.S.A. Taxonomy of Marine Bacteria: the Genus Beneckea PAUL BAUMANN, LINDA BAUMANN, AND M. MANDEL Department of Microbiology, University of Hawaii, Honolulu, Hawaii 96822, and Department of Biology, The University of Texas, M. D. Anderson Hospital and Tumor Institute at Houston, Houston, Texas 77025 Received for publication 5 April 1971 One-hundred-and-forty-five isolates of marine origin were submitted to an exten- sive physiological, nutritional, and morphological characterization. All strains were gram-negative, facultatively anaerobic, straight or curved rods which were motile by means of flagella. Glucose was fermented with the production of acid but no gas. Sodium but no organic growth factors were required. None of the strains were able to denitrify or fix molecular nitrogen. The results of nutritional and physiolog- ical tests were submitted to a numerical analysis. On the basis of phenotypic simi- larity, nine groups were established. These groups could be distinguished from one another by multiple, unrelated, phenotypic traits. Six groups which had deoxyri- bonucleic acid (DNA) containing 45 to 48 moles per cent guanine plus cytosine (GC) were assigned to a redefined genus Beneckea. All of the strains in this genus, when grown in liquid medium, had a single, polar flagellum. When grown on a solid medium, many strains had peritrichous flagella. Two groups were similar to previously described species and were designated B. alginolytica and B. natriegens. The remaining four groups were designated B. campbellii, B. neptuna, B. nereida, and B. pelagia. An additional group of phenotypically similar strains having the properties of the genus Beneckea was not included in the numerical analysis. These strains were readily separable from species of this genus and were designated B. parahaemolytica. Of the remaining groups, one was identified as Photobacterium flscheri. The other group (B-2) which had about 41 moles % GC content in its DNA could not be placed into existing genera. The main chemoorganotrophic bacterial flora sodium, gram-negative marine bacteria require of the sea, capable of growth on laboratory me- high concentrations of cations for the mainte- dia, is composed of gram-negative, straight and nance of the integrity of the cell wall (8, 15, 33, curved rods, which are motile by means of fla- 34). gella (27, 31, 33, 34, 43). A large body of litera- A large proportion of the gram-negative bac- ture (reviewed by MacLeod; 33, 34) indicates teria of marine origin ferment glucose with the that the growth of these organisms is dependent production of acid but no gas (10, 27, 31, 43) on the presence of sodium ion. This requirement Most of these organisms have been described as is specific and is independent of an osmotic func- polarly flagellated. A few have been reported to tion since growth does not occur in a medium in have polar flagella when grown in liquid medium which sodium is replaced by equimolar amounts and peritrichous flagella when grown on solid of other monovalent cations (33, 34). In the case medium (30, 31). The taxonomy of these orga- of two species of marine bacteria, it has been nisms is still poorly understood. Many have been shown that their permease systems require so- placed in Vibrio(3, 27, 47, 58), Aeromonas (36), dium for the uptake of exogenous substrates (17). Pseudomonas (10, 42), and Beneckea (7, 9). The sodium ion requirement of many or all Determinations of the guanine plus cytosine bacteria of marine origin has led to the sugges- (GC) content of the deoxyribonucleic acid tion that this property may serve to distinguish (DNA) of these strains have shown that the marine bacteria from soil and fresh water strains moles % GC ranges from 39-48 (5, 11, 13, 28, (33, 34). As yet, no comprehensive survey of the 32). Some of these organisms are pathogenic for sodium ion requirement of gram-negative bac- marine fish and shellfish (51). One species, V. teria from nonmarine sources has been per- parahaemolyticus, is pathogenic for man, causing formed. In addition to a specific requirement for an acute gastroenteritis (47). A common prop- 268 VOL. 107, 1971 GENUS BENECKEA 269 erty of these organisms is the ability to hydrolyze taining 0.2% (w/v) potassium lactate as the sole source chitin (3). During a study of the chitin-decom- of carbon and energy. posing, bacterial flora present in marine muds, Fermentation of carbohydrates. The ability of strains Campbell and Williams (10) isolated gram-neg- to ferment glucose was determined by the use of two different fermentation media. The first (F-l) differed ative rods which had either polar or peritrichous from YEB by containing 100 mM Tris-hydrochloride flagella and were able to ferment glucose with (pH 7.5), 1 g of Oxoid lonagar per liter, and 10 g of the production of acid but no gas. The polarly filter-sterilized glucose per liter. Portions (10 ml) of the flagellated strains were placed into the genus medium were dispensed into test tubes and inoculated Pseudomonas, the peritrichously flagellated by means of a stab. A control medium lacking glucose strains into the genus Achromobacter. The was also inoculated. About 5 ml of melted 10% (w/v) strains were screened for their ability to utilize a Oxoid lonagar, at 40 C, was added to make an agar relatively large number of carbon compounds as plug. The cultures were examined for turbidity and gas sole sources of carbon and energy. New species production for a period of 6 days. The second fermen- were tation medium (F-2) differed from F-I by containing 1 described and separated on the basis of a g of sodium thioglycolate per liter. The agar plug was few nutritional properties. The new species which omitted. F-2 medium containing glucose as well as a had been assigned to the genus Achromobacter control medium without glucose was inoculated and were subsequently placed into a newly created examined for growth on the surface and throughout the genus, Beneckea (7). medium at 24 and 48 hr. At the latter time, the pH of This study describes the properties of a collec- the culture was determined. tion of facultatively anaerobic, gram-negative, The ability of strains to produce acid from D-ribose, marine bacteria which are similar to the marine D-gluconate, D-mannitol, and glycerol under anaerobic strains which have been assigned to Vibrio, conditions was tested on fermentation media (F-3) which differed from BM by containing 25 mM Tris- Aeromonas, Pseudomonas, and Beneckea. The hydrochloride (pH 7.5), 0.5 g of Difco Yeast Extract results of our taxonomic analysis indicate that per liter, I g of Oxoid lonagar per liter, 2 ml of a 1.6% most of these organisms should be placed into (w/v) alcoholic solution of Brom Cresol Purple per liter, the redefined genus Beneckea. and 10 g of the filter-sterilized carbohydrate per liter. Subsequent procedures were identical to those for F-1. The cultures were examined for color change and gas MATERIALS AND METHODS production for a period of 6 days. The majority of the methods used in this study are Production of 2,3-butyleneglycol. Strains were those of Stanier et al. (57). Only significant modifica- grown in test tubes containing 10 ml of YEB with 1% tions as well as additional methods will be described. (w/v) D-glucose. After a 72-hr incubation, the Voges- Unless otherwise stated, all cultures were incubated at Proskauer (VP) test was performed (52). Quantitative 25 C. assays for acetoin or diacetyl, or both, as well as for Bacteriological media. The artificial sea water 2,3-butyleneglycol (39) were performed on all cultures *(ASW) used in this study consisted of 0.4 M NaCI, 0.1 which gave a positive VP test. M MgSO4*7H20, 0.02 M KCI, and 0.02 M Nitrogen metabolism. Strains were tested for their CaCl2 2H2O (34). The basal medium (BM) contained ability to denitrify (57). The medium used consisted of 50 mM tris(hydroxymethyl)aminomethane (Tris)-hy- YEB supplemented with 0.2% (v/v) glycerol, 3 g of drochloride (pH 7.5), 190 mM NH4C1, 0.33 mm NaNOs per liter, and 1 g of Oxoid lonagar per liter. K2HPO4g3H2O, 0.1 mM FeSO4 7H2O, and half- Each strain was first grown in the denitrification medium strength ASW (34). Basal medium agar (BMA) was under semianaerobic conditions. After 48 hr of incuba- prepared by separately sterilizing and then mixing tion, the cultures were tested for nitrite by the use of equal volumes of double-strength BM and 20 g of the starch-iodine spot test method (52). A loopful of Oxoid lonagar per liter. Yeast extract broth (YEB) the semianaerobic culture was then inoculated into a was made by supplementing BM with 5 g of Difco test tube containing homologous medium and was Yeast Extract per liter. Yeast extract agar (YEA) was sealed with an agar plug. Observations were continued prepared by solidifying YEB with 20 g of Difco Agar for 8 days. Cultures producing gas were scored positive per liter. In addition to the above complex media, for denitrification. Nitrogen fixation was tested by in- Difco Marine Agar (MA) was used. oculating cells from a fresh MA slant into BM from Tests for sodium and growth factor requirements. All which NH4Cl was omitted and which contained 0.2% of the strains were tested for their ability to grow on a (v/v) glycerol. Observations were continued for 6 days. minimal medium in the presence and absence of so- Extracellular enzymes.
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