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Home , Purple Bacteria, Rhodobacter, Rhodobacter capsulatus, Rhodocyclus, Rhodospirillaceae

INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, July 1984, p. 340-343 Vol. 34, No. 3 OO20-7713/84/030340-04$02.OO/O Copyright 0 1984, International Union of Microbiological Societies

Rearrangement of the and Genera of the Phototrophic ‘‘Purple Nonsulfur ”

J. F. IMHOFF,’* H. G. TRUPER,’ AND N. PFENNIG’ Institut fur Mikrobiologie, Rheinische Friedrich- Wilhelms-Universitat, 0-5300 Bonn, and Fachbereich Biologie, Universittit Konstanz, 0-1750 Konstanz,’ Federal Republic of Germany

A rearrangement of the species of the “purple nonsulfur bacteria” (Rhodospirillaceae)is proposed. The species with vesicular intracytoplasmic membranes are removed from the Rhodopseudornonas and are placed in the new genera and Rhodopila as (type species), , Rhodobacter sulfidophilus, Rhodobacter adriaticus, and (type species). gelatinosa and Rhodospirillum tenue are united with Rhodocyclirs purpureus (type species) in the genus Rhodocyclus as and . The decisions for this rearrangement were based mainly upon morphological and physiological properties; supporting arguments were based on structural similarities of macromolecular cell constituents.

Until now, primarily morphological properties have been phototrophic “relatives.” (The authorities to decide on the used to differentiate among the four genera of the Rhodospir- future basis of bacterial systematics are the International illaceae Pfennig and Truper 1971. Spiral-shaped bacteria Committee on Systematic Bacteriology and, perhaps the have been placed in the genus Rhodospirillum Molisch 1907, Judicial Commission of the International Committee on and spherical, ovoid, or rod-shaped bacteria have been Systematic Bacteriology.) The following points should be placed in the genus Rhodopseudomonas Kluyver and van emphasized: (i) the new genera are not necessarily homoge- Niel in Czurda and Maresch 1937. The genus Rhodomicro- neous with respect to genetic relatedness; (ii) changes are bium Duchow and Douglas 1949 was placed in the Rhodo- proposed only if they are supported by a number of indepen- spirillaceas in Bergey ’s Manual of Determinative Bacteriol- dent properties; and (iii) the decisions for rearrangement ogy, 8th ed. (22), on the basis of its phototrophic style of life were based upon the availability of distinguishing, easily and its characteristic peritrichously flagellated, stalk-form- recognizable morphological and physiological properties. ing cells. A fourth genus, Rhodocyclus Pfennig 1978, with Supporting arguments were taken from data on similarities in spiral-shaped, nonmotile cells, was described later. Much cytochrome c551 and c2 amino acid sequences (4, 5; R. P. new information has become available during the last few Ambler and T. E. Meyer, personal communications), DNA- years on the existing species (23), and a number of new rRNA hybridization (7, 8; M. Gillis et al., Abstr. IVth Int. species have been described, including Rhodopseudomonas Symp. Photosynthetic Procaryotes, A16, 1982), similarities sulfidophila Hansen and Veldkamp 1973, Rhodopseudo- in 16s rRNA oligonucleotide catalogs (11, 12, 24; E. Stacke- monas globiformis Pfennig 1974, Rhodopseudomonas sulfo- brandt and C. R. Woese, personal communication), lipid viridis Keppen and Gorlenko 1975, composition (M),lipopolysaccharide structure (1, 25), qui- Pfennig 1978, Rhodopseudomonas blastica Eckersley and none composition (15), and pathways of assimilation Dow 1981 (10, 19), Rhodospirillum salexigens Drews 1982 (14). (9, 20), Rhodopseudomonas rutila Akiba et al. 1983 (2), We propose the following: (i) to remove all species with Rhodopseudomonas marina Imhoff 1983 (16), and Rhodo- vesicular intracytoplasmic membranes from the genus Rho- pseudomonas adriatica Neutzling et al. 1984 (21a). dopseudomonas. According to Rules 39a and 39b of the Morphological, cytological, and physiological properties, International Code of Nomenclatue of Bacteria (21), the as well as recently accumulated data on the similarities of genus name Rhodopseudomonas has to be retained for those macromolecular structures show that the existing genera species that are grouped with Rhodopseudomonas palustris, comprise groups of species with widely differing properties, the type species of this genus; (ii) to place the removed which do not warrant classification within the same genus. species into two new genera, Rhodobacter gen. nov. and On the other hand, there are high degrees of similarity Rhodopila gen. nov.; and (iii) to unite the species Rhoda- between species of the phototrophic “purple nonsulfur bac- pseudomonas gelatinosa, Rhodospirillum tenue, and Rhoda- teria” and certain nonphototrophic species of gram-negative cyclus purpureus in one genus. According to Rule 44 of the procaryotes on the basis of the amino acid sequences of Znternational Code, the genus name has to be Rhodocyclus, cytochrome c molecules (3), deoxyribonucleic acid (DNA)- because Rhodocyclus purpureus is the only type species. ribosomal ribonucleic acid (rRNA) hybridization studies (7, Genus Rhodospirillum Molisch 1907 (emend. van Niel 1944). 8), and 16s rRNA oligonucleotide catalogs (11, 12, 24). Type species: Molisch 1907. Other Therefore, we believe that a rearrangement of the species species: Rhodospirillum photornetricum Molisch 1907, Rho- and genera of the purple nonsulfur bacteria is urgently dospirillum fulvum van Niel 1944, Rhodospirillum molis- needed to reach a better agreement between the taxonomic chianum Giesberger 1947, Rhodospirillurn salexigens Drews units and the established similarities of the species. Howev- 1982 (9, 20). Species removed from this genus: Rhodospiril- er, within a determinative taxonomic system the phototro- lum tenue Pfennig 1969. phic bacteria should be treated separately from their non- Cells are spiral shaped, 0.5 to 1.5 pm wide, and motile by means of polar flagella and contain intracytoplasmic photo- synthetic membranes as vesicles, lamellae, or stacks, but not * Corresponding author. as finger-like intrusions of the cytoplasmic membrane.

340 VOL. 34, 1984 NOTES 341

Cell shape and polar flagellation are the main common Rhodopseudomonas viridis have similar oligonucleotide cat- properties of this genus, which is in other aspects rather alogs. Hybridization studies of DNA and rRNA have led to heterogeneous. All species have different growth factor the arrangement of Rhodopseudomonas palustris, Rhodo- requirements. Rhodospirillum rirbrum and Rkodospirillum pseirdomonas viridis, and Rhodopseudomonas aridophila salexigens grow well under aerobic conditions in the dark, on one branch of “superfamily IV,” whereas Rhodopseudo- whereas the other species are very sensitive to oxygen. monas blastica is placed on another branch of this superfam- Three different types of intracytoplasmic membranes are ily together with the species included in the new genus present in the different species. Rhodo.spirillirm rirbrurn and Rhodobacter (see below). Because of its morphological Rhodospirillirm photometricirm have a large type of cyto- properties and since other conflicting results are lacking, chrome cz; the other species have a small type. The major Rhodopseudomonas blastica is retained in the genus Rho- are the same in Rhodospirillirmfrrl~~um and Rhodo- dopseudomonas. The recently described species Rhodo- spirillum molischianum (ubiquinone and menaquinone with pseudomonas rutila is classified with this genus on the basis a side chain of nine isoprenoid units), but different in all of its polar growth and budding, as well as its lamellar other species. Sulfate is reduced via 3’-phosphate adenosine intracytoplasmic membranes, which are parallel to the cyto- 5‘-phosphosulfate in Rhodospirilliim rubrum and Rhodospir- plasmic membrane. illum firlvum. Cell shape, mode of growth, and reproduction, as well as The heterogeneity of this genus may call for further the structure of the intracytoplasmic membranes, are the separation into several genera. However, this seems inap- characteristic properties that allow unequivocal classifica- propriate until more strains of each species are studied in tion of new species in this genus. detail and more data become available to justify the estab- Genus Rhodumicrobium Duchow and Douglas 1949. Type lishment of new genera. species: vannielii hchow and Douglas Genus Rhudupseudumunas Kluyver and van Niel in Czurda 1949. and Maresch 1937. Type species: Rhodopseirdomonas palus- Cells are ovoid, motile by peritrichous flagella, multiply tris (Molisch 1907) van Niel 1944. Other species: Rhodo- by budding, and have intracytoplasmic membranes parallel pseudomonas viridis Drews and Giesbrecht 1966, Rhodop- to the cytoplasmic membrane. Despite its similarity to seudomonas acidophila Pfennig 1969, Rhodopseirdomonas Rhodopseudomonas viridis and Rhodopseirdomonas acido- sulfoviridis Keppen and Gorlenko 1975, Rhodopseirdomonas philu with regard to cytochrome ct structure and 16s rRNA blastica Eckersley and Dow 1981 (10, 19), Rhodopseirdo- oligonucleotide composition, the genus Rhodomicrobium is monas rutila Akiba et al. 1983 (2), and Rhodopseudornonas maintained because of its characteristic morphological prop- marina Imhoff 1983 (16). Species removed from this genus: erties; these are peritrichous flagellation of the swarmer Rhodopseudomonas capsirluta (Molisch 1907) van Niel cells, the stalk, and exospore formation. Additional charac- 1944, Rhodopseudomonas sphaeroides van Niel 1944, Rho- teristics are the presence of unusual polar lipids, which are dopseirdomonus gelatinosa (Molisch 1907) van Niel 1944, similar to those of Rhodopila globiformis, and the differ- Rhodopseudomonas sdjidophilu Hansen and Veldkamp ences from Rhodopseudomonas and Rhodobacter based on 1973, Rhodopseudomonas globiformis Pfennig 1974, and DNA-rRNA hybridization studies. Rhodopseudomonas adviatica Neutzling et al. 1984. Genus Rhodopila gen. nov. The type species of Rhodopila Cells are rod shaped, show polar growth, asymmetrical gen. nov. (Rho.do.pi’la. Gr.n. rhodon rose; M. L. fem.n. division, or budding as a mode of reproduction, are motile by pila ball or sphere; M. L.fem.n. Rhodopila red-colored means of flagella, and have intracytoplasmic membranes that spherical bacterium) is Rhodopilu globijb-mis Pfennig 1974 are adjacent and parallel to the cytoplasmic membrane. comb. nov. Formerly this species has been included in the Growth factor requirements and sensitivity to oxygen are genus Rhodopseudomonas. different in the various species. Rhodopseudomonas viridis Cells are spherical to ovoid and motile by means of and Rhodopseudomonas acidophila have a small type of flagella, have vesicular intracytoplasmic membranes, and cytochrome cz; Rhodopseirdomonas palrrstris differs from grow only at low pH values. Biotin and p-aminobenzoic acid these species by containing different cytochromes and by the are required as growth factors. Cells are sensitive to oxygen, presence of a large type of cytochrome c?. The cytochrome but growth at low oxygen tensions in the dark is possible. structures of the other species in this genus are not known. The intracytoplasmic membrane structure is similar to that Studies of lipopolysaccharides have revealed 2,3-diamino- of Rhodobacter species, but a number of significant differ- 2,3-dideoxyglucose as an unique structural component of ences exist between these two genera. Rhodopila reduces Rhodop seudom on as viridis , R hodosp err domon as siiljo viri- adenosine 5 ‘ - p ho sphosul fate instead of 3 ‘-phosphate adeno- dis, and Rhodopseudomonas palustris, but not of Rhodo- sine 5’-phosphosulfate, has different , , pseudomonas mcrrina. Data on the lipopolysaccharide struc- and polar lipid compositions, and has a small cytochrome cf. tures of the other species are not available. The quinones It stands apart from Rhodobacter and Rhodopseudomonus present in the various species of this genus are also different. species according to DNA-rRNA hybridization studies and Rhodopseirdomonas palustris and Rhodopseirdomonas blas- 16s rRNA analyses, and it has in common with Rhodomicro- tica have Q-10 as the sole quinone component, whereas bium vannielii reduction of sulfate via adenosine 5‘-phospho- Rhodopseudomonas acidophila and Rhodopseudomonas sulfate, the presence of a small type of cytochrome Q, marina have MK-10 in addition. The quinones of the other substantial amounts of a high-potential iron- protein, species differ in the length of the isoprenoid chain. So far and the presence of unusual arninolipids as major compo- four species have been analyzed with respect to the pathway nents of the polar lipids. Therefore, Rhodopila is significant- of sulfate assimilation; Rhodopseudomonus palustris and ly different from all other genera and should be recognized as Rhodopseudomonas viridis reduce 3’-phosphate adenosine a separate genus. 5’-phosphosulfate, Rhodopseudomonas acidophilc reduces Genus Rhuducyclus Pfennig 1978. Type species: Rhodocy- adenosine 5’-phosphosulfate, and Rhodopseirdomonas Sid- clus pirrpureirs Pfennig 1978. Other species: Rhodocyclus foviridis is not able to reduce sulfate at all. From 16s rRNA gelatinosus (Molisch 1907) van Niel 1944 comb. nov. and studies it is known that Rhodopseudomonas palustris and Rhodocyclus tenuis Pfennig 1969 comb. nov. Formerly, 342 NOTES INT. J. SYST. BACTEHIOL.

Rhodocyclus tenuis has been included in the genus Rhodo- well-defined groups of both with spirillum as Rhodospirillum tenue, and Rhodocyclus - respect to phenotypic traits and with respect to similarity osus has been included in the genus Rhodopseudomonas as coefficients of 16s rRNA oligonucleotide catalogs; there- Rhodopseudomonas gelatinosa . fore, those latter two groups have been treated as true Cells are slender, curved, 0.3 to 0.7 km in diameter, and families with Latin family names (17). The group containing motile by means of polar flagella or nonmotile. Intracyto- the purple nonsulfur bacteria is a heterogeneous assemblage plasmic photosynthetic membranes are present in the form of phototrophic purple bacteria that do not form globules of of small finger-like intrusions of the cytoplasmic membrane. elemental sulfur inside their cells and do not grow at both Although the species of this genus formerly have been alkaline and highly saline conditions. Heterogeneity exists in included in three different genera, they show a remarkable the following two respects: (i) the three species of the new degree of similarity to each other and significant differences genus Rhodocyclus show a high degree of dissimilarity compared with all other species of the purple nonsulfur compared with the other genera of this group (see above) and bacteria. Rhodocyclus is the sole genus in this group that has may form a separate family in the future; and (ii) a growing only a few tubular intrusions of the cytoplasmic membrane number of species of the purple nonsulfur bacteria have 16s as intracytoplasmic photosynthetic membranes, cf/tochrome rRNA oligonucleotide catalogs that are more similar to those c551, an S-sulfocysteine synthase (13), and Q-8 and MK-8 as of certain nonphototrophic gram-negative bacteria than to major quinones. All three species reduce sulfate via adeno- those of other purple nonsulfur bacteria. Three examples are sine 5‘-phosphosulfate. According to DNA-rRNA hybridiza- the couples Rhodobacter capsulatus and Paracoccus deni- tion studies and 16s rRNA analyses they form a group that is trijicans, Rhodopseudomonas palustris and separate from all other purple nonsulfur bacteria. The results winogradskyi, and Rhodocyclus gelatinosus and Sphaeroti- of these analyses would allow establishment of different lus natans (12, 24). Therefore, we hesitated to continue to genera in a new family apart from the other purple nonsulfur use the family name Rhodospirillaceae for this group of bacteria. However, the species now placed in the genus phototrophic purple bacteria and assembled all potentially Rhodocyclus are surprisingly similar in a number of other phototrophic species and genera that do not belong to the properties. It is obvious that these species have to be placed and Ectothiorhodospiraceae in the group in a taxon separate from the other purple nonsulfur bacteria. called the purple nonsulfur bacteria. Because detailed determinative information is lacking to None of the strains or species of the purple nonsulfur safely distinguish them on the generic level, we propose bacteria which on the basis of other criteria would have to be placing them in the genus Rhodocycli4s. classified with this group forms globules of elemental sulfur Genus Rhodobucter gen. nov. The type species of Rhodo- inside its cells or grows under both alkaline and highly saline bacter gen. nov. (Rho.do.bac’ter. Gr.n. rhodon rose; M. conditions. In general, the cells of the species of purple L.masc.n. bacter equivalent of Gr.neut.n. bakterion rod; nonsulfur bacteria are smaller than those of the Chromati- M.L.masc.n. Rhodobacter red-colored rod) is Rhodobacter aceae. The cells are rod shaped, ovoid, spherical, or spiral capsulatus (Molisch 1907) van Niel 1944 comb. nov. Other shaped and motile or nonmotile. Motile forms have polar, species: Rhodobacter sphaeroides van Niel 1944 comb. subpolar, or peritrichous inserted flagella. No species is nov., Rhodobacter suljidophilus Hansen and Veldkamp 1973 known to contain gas vacuoles. Intracytoplasmic mem- comb. nov., and Rhodobacter adriaticus Neutzling et al. branes are present as vesicles, lamellar stacks, or occasional 1984 comb. nov. All species were formerly included in the tubular intrusions of the cytoplasmic membrane. Bacterio- genus Rhodopseudomonas. a or b and various may be present as All species of this genus have very similar properties. The photosynthetic pigments. cells are ovoid to rod shaped and motile or nonmotile, divide Some species are very sensitive to oxygen, whereas others by binary fission, and have vesicular photosynthetic mem- grow quite well under varying oxygen tensions in the light or branes. All species require thiamine, and most of them in the dark. Molecular nitrogen is fixed by nearly all of the require biotin and a different third vitamin as growth factors. species. Sulfide may or may not be oxidized to elemental The three species analyzed reduce sulfate via 3’-phosphate sulfur, sulfate, or both. Globules of elemental sulfur are adenosine 5’-phosqhosulfate. a and ca- never deposited within the cells. All species grow preferably rotenoids of the spheroidene group are present as photosyn- under phototrophic conditions with organic substances as thetic pigments. All species contain the large type of cyto- electron donors and carbon sources; most species require chrome c2 (Rhodobacter adriaticus has not been analyzed one or more growth factors, and the most frequently re- yet) and Q-10 as the sole quinone component. The species quired growth factors are biotin, thiamine, niacin, and p- are very similar according to 16s rRNA analyses and DNA- aminobenzoic acid. These compounds are rarely necessary rRNA hybridization studies. Differences occur in the oxida- as growth factors in the Chrornatiaceae or Ectothiorhodo- tion products of sulfide, which is oxidized by all four spiraceae, which may, however, require vitamin BI2 as a species. The species can also be differentiated by their lipid sole growth factor. The base composition of the DNA ranges compositions. Despite the small variation in their phenotypic from 61.8 to 72.4 mol% guanine plus cytosine. properties, DNA-DNA hybridization shows only a low de- In nature purple nonsulfur bacteria regularly occur in gree of homology among the DNA molecules of the different freshwater, brackish water, and marine habitats, as well as species. A study of 17 strains of Rhodobacter capsulatus, in moist soils and paddy fields. They rarely form reddish or Rhodobacter sphaeroides, and Rhodobacter sul$dophilus greenish water blooms, which may be characteristically revealed levels of homology of less than 30% (one exception formed, however, by most species of the other families of was a value of 40%) between DNA molecules of different anoxygenic phototrophic bacteria. species (6). Characterization of the purple nonsulfur bacteria. The ACKNOWLEDGMENTS species of the purple nansulfur bacteria are all members of We thank R. P. Ambler, T. E. Meyer, E. Stackebrandt, and C. R. the family Rhodospirillaceae (22). In contrast to this family, Woese for making unpublished data available to us and for critical the Chromatiaceae and the Ectothiorhodospiraceae are comments during preparation of the manuscript. VOL.34, 1984 NOTES 343

Some of our experimental results were obtained during work 13. Hensel, G., and H. G. Triiper. 1983. 0-acetylserine sulfyhydry- supported by a grant from the Deutsche Forschungsgemeinschaft. lase and S-sulfocysteine synthase activities of Rhodospirilfum tenue. Arch. Microbiol. 134:227-232. 14. Imhoff, J. F. 1982. Occurrence and evolutionary significance of LITERATURE CITED two sulfate assimilation pathways in the Rhodospirillaceue. 1. Ahamed, N. M., H. Mayer, H. Biebl, and J. Weckesser. 1982. Arch. Microbiol. 132:197-203. Lipopolysaccharide with 2,3-diamino-2,3-dideoxyglucosecon- 15. Imhoff, J. F. 1982. Taxonomic and phylogenetic implications of taining lipid A in Rhodopseudomonas sulfoviridis. FEMS Mi- lipid and quinone compositions in phototrophic microorga- crobiol. Lett. 14:7-30. nisms, p. 541-544. In J. F. G. M. Wintermans and P. J. C. 2. Akiba, T., R. Usami, and K. Horikoshi. 1983. 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