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Xanthobacter Flavus, a New Species of Nitrogen-Fixing Hydrogen Bacteria

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Xanthobacter Flavus, a New Species of Nitrogen-Fixing Hydrogen Bacteria INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Oct. 1979, p. 283-287 Vol. 29, No. 4 0020-7713/79/04-0283/05$02.00/0 Xanthobacter flavus, a New Species of Nitrogen-Fixing Hydrogen Bacteria K. A. MALIK AND D. CLAUS Deutsche Sammlung von Mikroorganismen, Gesellschaft fur Biotechnologische Forschung mbH, D-3400 Gottingen, Federal Republic of Germany Mycobacterium flavum strain 301 (= Deutsche Sammlung von Mikroorganis- men 338), a hydrogen-utilizing bacterium, is capable of fixing molecular nitrogen and resembles other nitrogen-fixing hydrogen bacteria. However, it is clearly different in many characters from other strains of M. flavum (Orla-Jensen) Jensen (syn.: Micro bacterium flavum Orla-Jensen). It does resemble strains of Xantho- bacter Wiegel et al. with respect to cell wall composition, production of carotenoid pigments, carbon source utilization pattern, and deoxyribonucleic acid (DNA) base composition (69 mol% guanine + cytosine). Strain 301 is here regarded as belonging to a new and distinct species, for which the name Xanthobacter flauus is proposed. Strain 301 is the type strain of this species. X. flavus differs from Xanthobacter autotrophicus, the only other species in this genus to date, in several respects, and the DNA-DNA hybridization between X. flavus and X. autotrophicus is only 25%. In 1961 Federov and Kalininskaya (13) iso- Tsukamura (24) showed that unlike most rap- lated an aerobic, nitrogen-fixing bacterium idly growing mycobacteria, strain 301 has no (strain 301) from turf podzol soils and identified mycobactin. Mycobacteria are usually gram pos- it according to Krasil’nikov’s scheme (18) as a itive and strongly acid fast, but strain 301 is member of Mycobacterium flavum (Orla-Jen- gram variable and weakly acid fast. Erickson sen) Jensen (syn.: Microbacterium flavum Orla- (12) reported that strain 301 has ubiquinone but Jensen). Subsequently, various authors (2-4, 6) no menaquinone, whereas most mycobacteria studied the nitrogen-fixing system of this strain, and other gram-positive organisms contain only which has also been included in comparative menaquinone. Erickson also reported that there studies (10,25) on nitrogen-fming hydrogen bac- are important differences between the respira- teria. tory system of strain 301 and those of mycobac- Even though Mycobacterium flavum and Mi- teria and that the electron transport system of crobacterium flavum are objective synonyms strain 301 is unique. (7-9, 17), there has been considerable confusion Thus, there has been considerable confusion between Mycobacterium flavum and strains regarding the taxonomic position of strain 301 identified as belonging to Microbacterium flu- (5, 10, 25), and it has been suggested that this uum, of which none of Orla-Jensen’s original strain is a member of the genus Corynebacte- strains are extant. For example, Biggins and rium (10). However, the taxonomy of the Cory- Postgate (5) showed that Mycobacterium flu- nebacteriaceae, especially those that are nitro- vum 301 differs from Microbacterium flavum gen-fixing bacteria, has been a subject of contro- National Collection of Industrial Bacteria versy itself. Biggins and Postgate (5) compared [NCIB] 8707 (= ATCC 10340 = Deutsche Mycobacterium flavum 301 with corynebacteria, Samlung von Mikroorganismen [DSM] 20296) arthrobacters, nocardiae, and mycobacteria and and stated that neither strain agrees with Orla- concluded that strain 301 should be reclassified. Jensen’s original description of Micro bacterium Wiegel et al. (25) extensively studied the ni- flavum (19). trogen-fming hydrogen bacteria and transferred Furthermore, Microbacterium flavum has a Corynebacterium autotrophicum Baumgarten cell wall structure of the “arabinose-galactose- et al. to a new genus, for which they proposed meso-diaminopimelic acid” type (22), whereas the name Xanthobacter. Howeve., :ID satisfac- the cell wall of Mycobacterium flavum has no tory recommendations have been made for arabinogalactone or mycolic acid. Micro bacte- strain 301, whose precise taxonomic position re- rium flavum has a deoxyribonucleic acid (DNA) mains unclear. base content of 58 to 59 mol% guanine plus Because strain 301 grows chemolithotrophi- cytosine (G+C), and Mycobacterium flavum 301 cally with hydrogen (10) and is capable of fixing has a G+C content of 69 mol% (5). molecular nitrogen, a taxonomic comparison of 283 284 MALIK AND CLAUS INT. J. SYST.BACTERIOL. this strain with Xantho bacter autotrophicus RESULTS AND DISCUSSION was indicated. This paper reports the results of In Table 1 are presented the main diagnostic this study. characters of Mycobacterium flavum 301 and X. autotrophicus. Both produce circular, entire, MATERIALS AND METHODS convex, and opaque colonies on nutrient agar. A comparison of the major characters shows that Bacterial strains. A culture of Mycobacterium M. flavum 301 is quite similar to X. autotrophi- flauum 301 (= DSM 338 = NCIB 10071) was obtained from the DSM and was characterized to confirm its cus. Strain 301, like X. autotrophicus DSM 432, authenticity. The identity of this strain was further grows well chemolithotrophically in a mineral confirmed by comparing it with a culture of Mycobac- medium in the presence of 60% Ha, 10% COz,2% terium flavurn 301 obtained from G. Zavarzin, Institute 02, and 28% Nz. of Microbiology, USSR Academy of Sciences, Mos- However, in contrast to X. autotrophicus cow. A culture of the type strain of X. autotrophicus, DSM 432, strain 301 cannot be grown repeatedly DSM 432, was also obtained from the DSM, as was a on synthetic media without added growth fac- culture of strain DSM 685, which was isolated from tors. The addition of 0.01% yeast extract (which garden soil at the DSM by K. A. Malik. can be replaced with vitamin solution) promotes Growth media. A standard mineral medium with the following composition was used for growing the the autotrophic growth of strain 301. strains: KH2P04, 2.3 g; NaeHP04.2He0, 2.9 g; NH4C1, X. autotrophicus DSM 432 and M. flavum 301 1.0 g; MgS04.7H20,0.5 g; CaC12. 2H20,0.01 g; Fe(NH4) can fix atmospheric nitrogen in nitrogen-defi- citrate, 0.05 g; trace element solution SL-6 of Pfennig cient media under reduced oxygen pressure, and (21), 6 ml; water, 1,OOO ml. both give a positive reaction in the acetylene For heterotrophic growth of the strains, this me- reduction test (3,4, 10,25). Many organic acids, dium was supplemented with carbon sources (0.2% e.g., acetic, citric, lactic, succinic, malic, fumaric, sugar or 0.1% organic acid, unless otherwise stated). gluconic, glutaric, and glutamic acids, are uti- For chemolithotrophic growth, 0.05% NaHC03 was lized by both strains. Carbohydrate utilization is added, and the cultures were incubated under an at- mosphere of 2% 02-10% C02-28% N2-60% H2. For very limited with X. autotrophicus DSM 432 growth on nitrogen-free medium, NHXl was omitted, (only fructose and sucrose are utilized) in com- 0.2% sodium succinate was added to the mineral me- parison to M. flavum 301. Methanol, ethanol, n- dium, and cultures were incubated under 2% 02and propanol, and n-butanol are utilized by both 98% Ne. strains. Methods. Growth factor requirements of the The cell shape of both M. flavum 301 and X. strains were determined according to the method of autotrophicus DSM 432 depends on the growth Holding and Collee (16). The standard mineral me- conditions. Large, irregularly branched cells dium was supplemented with the following: sodium were formed with media containing organic acids acetate, 0.1%; sodium lactate, 0.1%; sodium succinate, 0.1%; and glucose, 0.2%. When necessary, the standard and small rods were produced with sugar-con- medium was supplemented with the following vitamin taining media. Due to copious amounts of extra- solution: thiamine, riboflavin, nicotinic acid, pyrdoxin- cellular slime, the daughter cells are normally HC1, and calcium pantothenate, each at a concentra- held together after cell division, but no chains tion of 1 pg/ml, and vitamin BIZ, biotin, and folic acid, are formed. Within the cells, poly-/I-hydroxy- each at 0.1 pg/ml. butyrate refractile bodies can be observed. The utilization of compounds as sole sources of Wiegel et al. (25) reported that M. flavum 301 carbon was tested on agar plates by the method de- and X. autotrophicus DSM 432 resemble each scribed by Stanier et al. (23). other in that neither contains arabinogalactan, DNA base composition and hybridization. For mycolic acids, or menaquinones and in that they DNA preparations, the strains were grown on Difco nutrient broth containing 0.2% succinate. The method have ubiquinones, the same fatty acid pattern, of Gillis et al. (15) was used for the purification of and similar carotenoid pigments (12). DNA and the determination of DNA base composi- According to Biggins and Postgate (5), broken tion. DNA hybridization was determined optically by suspensions of Microbacterium flavum NCIB the renaturation rate method of De Ley et al. (11). 8707 gave no reaction on Ouchterlony (20) plates The degree of binding was calculated according to the against antiserum to Mycobacterium flavum formula of De Ley et al. (11). 301, whereas a broken suspension of M. flavum Immunological cross-reactions. Antisera to 301 gave six precipitation lines. whole cells of M. flavum 301, Azotobacter vinelandii Three wild-type X. autotrophicus strains ATCC 13705 (= DSM 366), and X. autotrophicus strains DSM 431, 432, and 1393 were obtained from (DSM 431,432, and 1393) have a few antigens in rabbits by conventional procedures. Crude serum was
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