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Intra- and Intergeneric Similarities of Ribosomal Ribonucleic Acid Cistrons of Free-Living, Nitrogen-Fixing Bacteria

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Intra- and Intergeneric Similarities of Ribosomal Ribonucleic Acid Cistrons of Free-Living, Nitrogen-Fixing Bacteria INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1980, p. 106- 122 Vol. 30, No. 1 oO20-7713/80/01-01O6/17$02.oO/0 Intra- and Intergeneric Similarities of Ribosomal Ribonucleic Acid Cistrons of Free-Living, Nitrogen-Fixing Bacteria J. DE SMEDT, M. BAUWENS, R. TYTGAT, AND J. DE LEY Laboratorium uoor Microbiologie en Microbiele Genetica, Faculteit der Wetenschappen, Rijksuniuersiteit, B-9000 Gent, Belgium ‘*C-labeledribosomal ribonucleic acid (rRNA) was prepared from Azoto bacter chroococcum NCIB 8002, Azotobacter paspali 8A, Azomonas agilis NCIB 8636, Azomonas insignis WR 30, Beuerinckia indica NCIB 8712, and Azospirillum brasilense ATCC 29145. These rRNA’s were hybridized under stringent condi- tions with filter-fixed deoxyribonucleic acid from a great variety of gram-negative bacteria. Each hybrid was described by: (i) the temperature at which 50% of the hybrid was denatured, and (ii) the percent rRNA binding (amount in micrograms of rRNA duplexed to 100 pg of deoxyribonucleic acid). These data were used to construct rRNA similarity maps. The following conclusions could be drawn concerning rRNA cistron similarities. (i) Bacterial genera with free-living, aerobic, nitrogen-fixing members are very diverse and belong to different rRNA superfam- ilies. The present family Azotobacteriaceae is not a biological unit, and its status as a family is highly questionable. (ii) Azotobacter chroococcum, Azoto bacter vinelandii, Azoto bacter beijerinckii, Azoto bacter paspali, Azoto bacter miscel- lum, Azotobacter armeniae, and Azotobacter nigricans belong in the genus Azotobacter. Any synonymy of these names remains to be determined. Azomonas agilis, Azomonas insignis, and Azomonas macrocytogenes constitute indepen- dent branches, which are about equidistant from Azotobacter and section I of Pseudomonas as presented in Bergey ’s Manual of Determinative Bacteriology, 8th ed. Xanthomonas, Alteromonas vaga, and Alteromonas communis are lo- cated in the same rRNA superfamily. (iii) The genus Beijerinckia appears to be rather heterogeneous. Its closest relatives appear to be Xantho bacter autotro- phicus, “Mycobacterium”flavum, “Pseudomonas” azotocolligans, “Pseudomo- nas” diminuta, the authentic rhodopseudomonads, and some other organisms. These organisms belong in the same rRNA superfamily as Azospirillum, Agro- bacterium, Rhizo bium, Aceto bacter, Gluconobacter, and Zymomonas. (iv)Derxia belongs in still another rRNA superfamily, together with Chromobacterium, Janthinobacterium, the Pseudomonas acidovorans and Pseudomonas solana- cearum groups, Alcalienes, and a few other taxa. (v) The following organisms were generically misnamed: “Azomonas insignis” ATCC 12523, “Mycobacte- rium” flavum 301, “Pseudomonas” azotocolligans ATCC 12417, “Pseudomonas” diminuta CCEB 513, and “Rhodopseudomonas” gelatinosa (all strains exam- ined). Molecular biological methods, such as deoxy- correlation between the degree of rRNA similar- ribonucleic acid (DNA)-DNA or DNA-ribo- ity and the overall phenotypic similarity of bac- somal ribonucleic acid (rRNA) hybridizations, terial genera (19,23). Similarity between rRNA which directly compare bacterial genomes, have cistrons appears to be a.good criterion for the opened new perspectives for bacterial classifi- classification of bacteria on generic and supra- cation. Many bacterial genera are phylogeneti- generic levels. In this paper we attempt to clarify cdy too far removed from each other to form the intra- and intergeneric relationships of sev- stable DNA-DNA hybrids. DNA-DNA hybridi- eral Nz-fixing bacterial taxa through DNA- zations are useful either within a genus, such as rRNA hybridizations. Agrobacterium (ZO), or between genera which Until now classification within the family have not diverged too much, such as in the Azoto bacteriaceae has been based mainly on Enterobacteriaceae (12; D. Izard, C. Ferragut, phenotypic features (13,31).Only one molecular and H. Leclerc, in press). rRNA’s are conserva- biologkal character, namely DNA base compo- tive molecules (25, 36, 43). There is a good sition (guanine plus cytosine [G+C) content), 106 VOL. 30,1980 rRNA CISTRONS OF NITROGEN-FIXING BACTERIA 107 has been examined (15,18).In Bergey’s Manual plating and by microscopic examination of living and of Determinative Bacteriology, 8th ed. (13), Gram-stained cells. Mass cultures were grown in Roux these characters were used to distinguish four flasks on media described previously (23). On a solid genera in this family. The genus Azotobacter, medium, Azotobacter chroococcum NCIB 8002 and NCIB 8003 and Derxia gummosa NCIB 9064 pro- which was established by Beijerinck (7),consists duced too much slime, thus preventing harvesting of of cyst-forming free-living, aerobic, gram-nega- the cells. These two organisms were grown in liquid tive, nitrogen-fixing bacteria with 63 to 66 mol% culture in broad-bottomed Erlenmeyer flasks; shaking G+C content. Winogradsky (49) proposed in- provided good aeration. The Xanthobacter autotro- cluding the Azotobacter species that do not form phicus and “Mycobacteriurn” flavum strains were thick-walled cysts in a new genus, Azomonas; grown in the laboratory of H. G. Schlegel. We received the G+C values of members of this genus range them as freeze-dried cell powders. from 53 to 59 mol%. Starkey and De (41) isolated Preparation of high-molecular-weight DNA. DNA samples were prepared by the method described from Indian rice field soils a nitrogen-fming or- by Marmur (35). They were purified by CsCl gradient ganism which they named Azotobacter indicum. centrifugation, denatured, and fmed on cellulose ni- Because of its morphological and physiological trate membrane filters as described previously (17,23). differences from other Azoto bacter species, Derx Preparationof [“C]rRNA. Radioactively labeled (21) proposed including this species in a new rRNA was prepared as described previously (17, 23), genus, Beijerinckia; its G+C content ranges using [2-’4C]uracilas precursor. The specific activities from 55 to 61 mol%. The genus Derxia was of these rRNA’s were as follows: 9,898 and 9,997 cpm/ proposed by Jensen et al. (32) for the nitrogen- pg for the 23s and 16s fractions of Azotobacter chroo- fixing organism they isolated from West Bengal coccum NCIB 8002, respectively; 13,646 and 14,336 soil and which appeared different in many fea- cpm/pg for the 23s and 16s fractions of Azotobacter paspali 8A, respectively; 14,989 and 15,698 cpm/pg for tures from all previously known nitrogen-fixing the 23s and 16s fractions of Azomonas agilis NCIB strains. They included it in the Azotobacteri- 8636, respectively; and 6,704 and 6,398 cpm/pg for the aceae because of its capacity to fm large amounts 23s and 16s fractions of Azomonas insignis WR 30, of nitrogen. Its G+C content ranges from 69 to respectively. Beijerinckia indica NCIB 8712 and 72 mol%. We performed DNA-rRNA hybridiza- Azospirillum brasilense ATCC 29145 did not incor- tions between labeled reference rRNA’s from porate [2-I4C]uracil.With [6-“C]orotate as a precursor Azoto bacter chroococcum,Azotobacter paspali, for labeling, the rRNA of B. indica NCIB 8712 had Azomonas agilis, Azomonas insignis, and Bei- specific activities of 1,015 and 959 cpm/pg for the 23s jerinckia indica strains and the DNA of a great and 16s fractions, respectively, whereas the rRNA of Azospirillum brasilense ATCC 29145 had specific ac- variety of bacteria to measure the similarity of tivities of 2,267 and 2,300 cpm/pg for the 23s and 16s their rRNA cistrons and to establish the degree fractions. B. indica NCIB 8712 and Azospirillum of heterogeneity within the family Azotobacter- ATCC 29145 were selected because they are the type iaceae. strains of their respective species (13,44), and the four We also performed hybridizations with refer- other strains were selected because they were among ence rRNA from Azospirillum brasilense. Azos- the oldest available in their taxa. Azotobacter chroo- pirilla have been isolated from the rhizospheres coccum NCIB 8002 appears to be the original Azo- of a variety of grasses, legumes, and grain crops monas strain 1 of Winogradsky (9). Azotobacter pas- and from soils in tropical and temperate regions; pali 8A, kindly provided by J. Dobereiner, was one of the original strains of Dobereiner. Azomonas agilis they attracted special attention because of their NCIB 8636 is one of the strains of J. Smit (9). Azo- ability to fix nitrogen (24). The name Azospiril- monas insignis WR 30 was strain 8 of V. Jensen and Zum was recently proposed by Tarrand et al. was isolated in 1954 (J. P. Thompson, personal com- (44). The genus contains two species, Azospiril- munication). lum lip0ferum and Azospirillum brasilense. We Hybridizations. Hybridizations, ribonuclease included the type strain (ATCC 29145) of Azo- treatments, and thermal stability measurements of the spirillum brasilense and a reference strain hybrids were performed as described previously (17, (SpBrl7) of Azospirillum lipoferum in the pres- 23). Hybridizations were carried out in 2X sodium ent study in order to determine the taxonomic saline citrate buffer (lx sodium saline citrate buffer is 0.15 NaCl plus 0.015 M sodium citrate), pH 7.0 con- position of Azospirillum. taining 20% formamide at the stringent temperature We also examined some other free-living, NS- of 50°C (17). For the experiments with the rRNA of fixing bacteria, such as Xanthobacter autotro- B. indica NCIB 8712, a slight modification was needed phicus, “Mycobacterium” flavum, and some because of the low specific activity;
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