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Home , Bacterial taxonomy, Beijerinckia, Bordetella, Buttiauxella, Cedecea, Chromatiaceae

INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, July 1988, p. 321-325 Vol. 38, No. 3 0020-7713/88/03032 1-05$02.OOtO Copyright 0 1988, International Union of Microbiological Societies

Proteobacteria classis nov. a Name for the Phylogenetic Taxon That Includes the “Purple and Their Relatives”

E. STACKEBRANDT,l R. G. E. MURRAY,2* AND H. G. TRUPER3 Lehrstuhl fur Allgemeine Mikrobiologie, Biologiezentrum, Christian-Albrechts Universitat, 2300 Kid, Federal Republic of ’; Department of and Immunology, University of Western Ontario, London, Ontario, Canada N6A 5C12; and Institut fur Mikrobiulogie, Universitat Bonn, 5300 Bonn I, Federal Republic of Germany3

Proteobacteria classis nov. is suggested as the name for a new higher taxon to circumscribe the a, p, y, and 6 groups that are included among the phylogenetic relatives of the purple photosynthetic bacteria and as a suitable collective name for reference to that group. The group names (alpha, etc.) remain as vernacular terms at the level of subclass pending further studies and nomenclatural proposals.

Phylogenetic interpretations derived from the study of the interim while the phylogenetic data are being integrated ribosomal ribonucleic acid (rRNA) sequences and oligonu- into formal bacterial . It does not appear to be cleotide catalogs provide an important factual base for inappropriate or confusing to use the protean prefix because arrangements of higher taxa of bacteria (25, 26). A recent of the Proteus among the Proteobacteria; the reasons workshop organized by the International Committee on for use are clear enough. Systematic Bacteriology recognized that a particularly di- This new class is so far only definable in phylogenetic verse but related group of gram-negative bacteria, including terms. Above all, it is shown by the evolutionary distance phototrophic and heterotrophic bacteria, needed a formal matrix generated from homologies of complete 16s rRNAs, collective name (22). These are often referred to from which a is derived. According to as “ and their relatives,” and this is not Woese (25) a corresponding tree given by maximum parsi- appropriate because most of them are not purple or photo- mony of sequence selection recognizing unique nucleotides synthetic. We believe that they should be named at the level at specific sites results in a very similar topography. Few of class. class-specific signature nucleotides of the 16s rRNA are This group has evolved relatively rapidly to generate a determinable compared with those found in other major lines number of branches, including organisms of great biological of descent of the (25). There is a preference for significance but startlingly different physiological attributes . adenine at position 906 and for cytosine at position 1520 (a These relationships invalidate the proposal for an interim set guanine residue is the eubacterial consensus composition at of higher taxa proposed in Bergey’s Munual of Systematic these positions). In terms of ribonuclease T,-resistant oligo- Bacteriology (14) separating the classes Scotobacteria (for nucleotides, catalogs of Proteobncteria can be characterized nonphotosynthetic true bacteria, which now prove to be by the following signatures (positions and distribution in relatives of purple bacteria) and Anoxyphotobacteria (en- parentheses): CUAAUACCG (170; alpha-delta), YCAC compassing the photosynthetic bacteria having photosystem AYYG (315; alpha-delta; Y = pyrimidine), AAUUUUG or I alone, including the purple bacteria). The remaining class, AAUUUUC (365; alpha-delta), CUAACUYYG (510; alpha, Oxyphotobacteria, can be retained as a phylogenetically gamma, delta), and UCACACCAUG (1410; alpha-delta). valid circumscription of the bacteria having both photosys- The alpha, beta, and gamma groups correspond to rRNA tems I and 11. These and the other gram-negative bacteria superfamilies IV, 111, and I+II, respectively, as defined by forming the major phylogenetic group derived from the main De Ley and co-workers (3-6, 9, 11, 15, 16) on the basis of stem of bacterial evolution can still be conveniently classi- rRNA similarities (members of the delta subclass have not fied as members of the division Gracilicutes until further yet been included in such studies). The groups within the phylogenetic studies clarify some of the orders of branching Proteobacteria are termed “subdivisions” by Woese et al., or the need for status at the level of division. The gram- (26) or “subphyla” by Woese (25). Only a comparison of full positive bacteria form a more clearly structured phyloge- 16s rRNA sequences can be expected to convincingly netic group and can remain, as recommended (22), assem- determine the common origin of the four subclasses; other bled in the division . methods, such as deoxyribonucleic acid-rRNA pairing, com- The outstanding attribute of the major phylogenetic parison of 5s rRNA sequences, and 16s rRNA cataloging, branches (a,p, y, and 6) within the purple bacteria and their are not capable of discrimination at that level. relatives is the diversity of shape and physiology. Therefore, Table 1 lists those taxa which have been found to be we propose that these organisms be designated Proteobac- members of each of the individual groups, and the methods teria classis nov. (Prot.e.0.bac.ter’i.a. Gr. n. Proteus, a that determine their phylogenetic positions are indicated in Greek god of the sea, capable of assuming many different the references cited; the names used are included without shapes; Gr. dim. n. bakterion, a small rod; Proteobacteria prejudice. At this time we do not have a formal nomencla- protean group of bacteria of diverse properties despite a tural proposal for any new ranks between class and genus common ancestry). It seems appropriate to use the suffix because thorough study will be required to establish stable -bacteria at this hierarchical level because it is consistent taxonomic arrangements and phenotypic markers for those with an extant proposal of higher taxa (14) that is useful in ranks (22). The groups corresponding to the immediate separations within the Proteobncteria should be at the subclass rank and are so shown in Table 1; however, to * Corresponding author. emphasize that these group names have no formal status in

321 322 NOTES INT. J. SYST.BACTERIOL.

TABLE 1. Genera recognized as members of the class Proteobacteria“ References Subclass Taxonb 16s rRNA 16s rRNA-23s rRNA 5s rRNA sequences hybridization sequences “Alpha” Rhodohacter 25 9 Rhodomicrobium 25 Rhodopseudomonas 25 9 Rhodopila 25 Rhodospirillum 25 9 13 Acetobacter 9 Acidiphilium 13 Agrobacteriurn 25 9 Ancalornicrobium N P” Aquaspirillum 25 9 Azospirillurn 25 9 Beijerinckia NP 9 Blastobacter 17 Brady rh izo bium 8 9 Caulobacter NP Erythrobacter 25 Filornicrobium 17a Gemmobacter 17 Gluconohacter 9 Hyp homic ro biurn 17a 17a Hyphornonas 17a Me thy lobacteriurn NP My coplana Nitrobacter 25 17a Paracoccus 25 13 Pedornicrobium 17a Phy llobacterium Phenylobacterium 25 Prosthecornicrobium NP Rhizohium 25 Rochalimaea 25 Stella 17a NP Xanthobacter NP Zymornonas 9

“Beta” R hodocyclus 25 13 Achromohacter 11 4 Alcaligenes 25 15 Bordetella 15 Aquaspirillum 25 Chrornobacteriurn 25 5 Comamonas 25 6 Derxia NP 5 Janthinobacterium 25 5 King ella 16 Leptothrix 19 Methylomonas Clara 28 Methanolomonas 28 Methanomonas 28 25 16 25 Nitrosolobus 25 Nitrosospira 25 Nitrosovibrio 25 15 Pseudornonas acidovorans complex 25 5 Pseudornonas solanacearum complex 25 5 13 Sirnonsiella NP Sphaerotilus 25 Spirill urn 25 Tuy lorella 15 Thiobucillusd 25 19 Vitreoscilla 25 19 Xylophilus 24

Continued on following page VOL. 38, 1988 NOTES 323

TABLE 1-Continued References Subclass Taxonb 16s rRNA 16s rRNA-23s rRNA 5s rRNA sequences hybridization sequences "Gamma" Chrornatiaceae 25 Amoehohacter 7 Chrornatiurn 25 13 Larnprocystis 25 Thiocapsa 25 Thiocystis 25 Thiodictyon 25 Thiosp irill urn 25 25 Eciothiorhodospira 25 Acinetobacter 25 16 Aeromonadaceae 3 Aerornonas 27 3 Alterornonas 27 3 13 Alysiella NP Azornonas 5 5 Beggiatoa 25 19 Branhamella 16 Deleya NP 5 Enterohacteriaceae 27 3 Budvicia (1) Buttiauxella' Cedecea" Citrobacter" Edwardsiella' Enterohacter 27 Erwinia' Es ch e ric h ia 27 3 Hafnia' ' Kluyvera' Leclercia (21) Leminorella' Moellerella' Morganella' Obesurnbacterium' Proteus 27 Providencia' Rahnella' '' 27 " Taturnella' 27 Yokenella (= Koserella) (12) Xenorhabdus 6a Frateuria 5 Halornonas 27 Legionella 27 Leucothrix 27 Lysohacter 27 Marinornonas 5 Moraxella 16 Oceanospirillurn 25 Pasteurellaceue 3 Pasteurella 25 3 Plesiornonas 3 juorescens complex 25 5 13 (10) Ruminobacter 18, 25 Serpens 25 Thiorn icrospira 19 19

Continued on following page 324 NOTES INT. J. SYST.BACTERIOL.

TABLE 1-Con tin lied References Subclass Taxon” 16s rRNA 16.5 rRNA-23s rRNA 5s rRNA sequences hybridization sequences acea e 3 3 Enhydrobacter (20) Listonella 27 Photobacterium 27 3 Skewanella Xanthomonas 25 5 Xy lella 23

‘‘Delta’ ’ Bdellovibrio 25 Desulfobucter 25 Desulfobulbus 25 Desulfococcus 25 Desulfonema 25 Desulfovibrio 25 Desulfuromonas 25 Myxococcuceae 2s Chondromyces NP 25 Myxococcits 25 Nannocystis 25 Sorangium 25 Stigmatella 25 Pelobacter NP ‘’ Genera of phototrophic bacteria head the list of taxa and are followed by other taxa in alphabetical order. Only phylogenetically defined families are included. References are not necessarily to the original presentation of data but are selected sources giving more comprehensive overviews. The subclasses “alpha” to “gamma” contain many misclassified strains which are not listed but which can be recognized in the original literature. ’The numbers in parentheses are reference numbers. I’ NP, Unpublished data of Stackebrandt and co-workers. Heterogeneous genus. Genera assigned to the Enterobacieririceae by deoxyribonucleic acid hybridization data and not by rRNA sequencing (2). nomenclature, they are put in quotation marks and not set in Appl. Microbiol. 10:121-125. italic type. A few genera have been effectively aligned within 7. Fowler, V. J., N. Pfennig, W. Schubert, and E. Stackebrandt. a group (e.g., as a family), and this is indicated by direct 1984. Towards a phylogeny of phototrophic purple sulfur bac- reference without assignment of method. It would be appro- teria: 16s rRNA oligonucleotide cataloguing of eleven of priate to refer to a named as belonging to, for . Arch. Microbiol. 139:382-387. 8. Hennecke, H., K. Kaluza, B. Thony, M. Fuhrmann, W. Ludwig, example, the Proteobucteriu alpha group. and E. Stackebrandt. 1985. Convergent evolution of nitrogenase genes and 16s rRNA in species and other nitrogen- LITERATURE CITED fixing bacteria. Arch. Microbiol. 142:342-348. 9. Jarvis, B. D. W., M. Gillis, and J. De Ley. 1986. Intra- and 1. Bouvet, 0. M. M., P. A. D. Grimont, C. Richard, E. Aldova, 0. intergeneric similarities between the ribosomal ribonucleic acid Hausner, and M. Gabrhelova. 1985. Budvicia aquatica gen. cistrons of Rhizobium and Bradyrhizobium species and some nov., sp. nov.: a hydrogen sulfide-producing member of the related bacteria. Int. J. Syst. Bacteriol. 36:129-138. En?erobac?eriaceae. Int. J. Syst. Bacteriol. 3560-64. 10. Juni, E., and G. A. Heym. 1986. Psychrobacter immobilis gen. 2. Brenner, D. J. 1984. Family I. , p. 409-601. nov., sp. nov.: genospecies composed of gram-negative, aero- In N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of bic, oxidase-positive coccobacilli. Int. J. Syst. Bacteriol. 36: systematic bacteriology, vol. 1. The Williams & Wilkins Co., 388-391. Baltimore. 11. Kersters, K., K.-H. Hinz, A. Hertle, P. Segers, A. Lievens, 0. 3. Colwell, R. R., M. T. MacDonell, and J. De Ley. 1986. Proposal Siegmann, and J. De Ley. 1984. sp. nov., to recognize the family Aeromonaduceae fam. nov. Int. J. Syst. isolated from the respiratory tracts of turkeys and other birds. Bacteriol. 36:473477. Int. J. Syst. Bacteriol. 3456-70. 4. De Ley, J., P. Segers, K. Kersters, W. Mannheim, and A. 12. Kosako, Y., R. Sakazaki, G. P. Huntley-Carter, and J. J. Farmer Lievens. 1986. Intra- and intergeneric similarities of the Borde- 111. 1986. Yokenella regensburgei and Koserella trabulsii are tella ribosomal ribonucleic acid cistrons: proposal for a new subjective synonyms. Int. J. Syst. Bacteriol. 33:127-129. family, Alcaligenaceae. Int. J. Syst. Bacteriol. 36:405414. 13. Lane, D. J., D. A. Stahl, G. J. Olsen, D. J. Heller, and N. R. 5. De Vos, P., M. Goor, M. Gillis, and J. De Ley. 1985. Ribosomal Pace. 1985. Phylogenetic analysis of the genera Thiobacillus and ribonucleic acid cistron similarities of phytopathogenic Pseudo- Thiomicrospiru by 5s rRNA sequences. J. Bacteriol. 163:75- species. Int. J. Syst. Bacteriol. 35169-184. 81. 6. De Vos, P., K. Kersters, E. Falsen, B. Pot, M. Gillis, P. Segers, 14. Murray, R. G. E. 1984. The higher taxa, or, a place for and J. De Ley. 1985. Comamonas Davis and Park 1962 gen. everything . . .?, p. 33. In N. R. Krieg and J. G. Holt (ed.), nov., nom. rev. emend., and Comamonas terrigena Hugh 1962 Bergey’s manual of systematic bacteriology, vol. 1. The Wil- sp. nov., nom. rev. Int. J. Syst. Bacteriol. 35443-453. liams & Wilkins Co., Baltimore. 6a.Ehlers, U. R., U. Wyss, and E. Stackebrandt. 1988. 16s rRNA 15. Rossau, R., K. Kersters, E. Falsen, E. Jantzen, P. Segers, A. cataloging and the phylogenetic position of Xenorhabdus. Syst. Union, L. Nehls, and J. De Ley. 1987. Oligella, a new genus VOL. 38, 1988 NOTES 325

including comb. nov. (formerly Moraxella 21. Tamura, K., R. Sakazaki, Y. Kosako, and E. Yoshizaki. 1986. urethralis) and sp. nov. (formerly CDC Leclercia adecarboxylata gen. nov., comb. nov., formerly group We): relationship to equigenitalis and related known as Escherichia adecarboxylata. Curr. Microbiol. 13: taxa. Int. J. Syst. Bacteriol. 37:198-210. 179-194. 16. Rossau, R., A. Van Landschoot, W. Mannheim, and J. De Ley. 22. Wayne, L. G., D. J. Brenner, R. R. Colwell, P. A. D. Grimont, 1986. Inter- and intrageneric similarities of ribosomal ribonu- 0. Kandler, M. I. Krichevsky, L. H. Moore, W. E. C. Moore, cleic acid cistrons of the . Int. J. Syst. Bacteriol. R. G. E. Murray, E. Stackebrandt, M. P. Starr, and H. G. 36:323-332. Triiper. 1987. Report of the ad hoc Committee on Reconciliation 17. Rothe, B., A. Fischer, P. Hirsch, M. Sittig, and E. Stackebrandt. of Approaches to Bacterial Systematics. Int. J. Syst. Bacteriol. 1987. The phylogenetic position of the budding bacteria Blasto- 37:463464. bacter aggregatus and Gernrnobacter aquatilis gen. nov., sp. 23. Wells, J. M., B. C. Raju, H.-Y. Hung, W. G. Weisburg, L. nov. Arch. Microbiol. 147:92-99. Mandelco-Paul, and D. J. Brenner. 1987. Xylella fastidiosa gen. 17a.Stackebrandt, E., A. Fischer, T. Roggentin, U. Wehmeyer, D. nov., sp. nov. : gram-negative, xylem-limited, fastidious Bomar, and J. Smida. 1988. A phylogenetic survey of budding, bacteria related to Xanthomonas spp. Int. J. Syst. Bacteriol. and/or prosthecate, nonphototrophic eubacteria: membership of 37:136-143. Hyphornicrobiurn, Hyphornonas, Pedomicrobiurn, Filornicm- 24. Willems, A., M. Gillis, K. Kerster, L. Van den Broecke, and J. biurn, Caulobacter, and “Dichotomicrobium” to the alpha De Ley. 1987. Transfer of Xanthornonas ampelina Panagopoulos subdivision of purple non-sulfur bacteria. Arch. Microbiol. 149: 1969 to a new genus, Xylophilus gen. nov., as Xylophilus 547-556. ampelinus (Panagopoulos 1969) comb. nov. Int. J. Syst. Bacte- 18. Stackebrandt, E., and H. Hippe. 1986. Transfer of Bactcroides rial. 37:422430. arnylophilus to a new genus Rurninobacter gen. nov., nom. rev. 25. Woese, C. R. 1987. Bacterial evolution. Microbiol. Rev. as Rurninobacter arnylophilus comb. nov. Syst. Appl. Micro- 51:221-271. biol. 8:204207. 26. Woese, C. R., E. Stackebrandt, R. J. Macke, and G. E. Fox. 19. Stahl, D. A., D. J. Lane, G. J. Olsen, D. J. Heller, T. M. 1985. A phylogenetic definition of the major eubacterial taxa. Schmidt, and N. R. Pace. 1987. Phylogenetic analysis of certain Syst. Appl. Microbiol. 6:143-151. sulfide-oxidizing and related morphologically conspicuous bac- 27. Woese, C. R., W. G. Weisburg, C. M. Hahn, B. J. Paster, L. B. teria by 5s ribosomal ribonucleic acid sequences. Int. J. Syst. Zablen, B. J. Lewis, T. J. Macke, W. Ludwig, and E. Stacke- Bacteriol. 37:116-122. brandt. 1985. The phylogeny of purple bacteria: the gamma 20. Staley, J. T., R. L. Irgens, and D. J. Brenner. 1987. Enhydro- subdivision. Syst. Appl. Microbiol. 6:25-33. hacter aerosaccus gen. nov., sp. nov., a gas-vacuolated, facul- 28. Wolfrum, T., and H. Stolp. 1987. Comparative studies on 5s tatively anaerobic, heterotrophic rod. Int. J. Syst. Bacteriol. RNA sequences of RUMP-type methylotrophic bacteria. Syst. 37:289-291. Appl. Microbiol. 9:273-276.