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Request for an Opinion |
Landcare Research, Private Bag 92170, Auckland, New Zealand
Correspondence
J. M. Young
youngj{at}LandcareResearch.co.nz
ABSTRACT
The synonymy of the genera Ensifer and Sinorhizobium was recently reported, but it was proposed that the later-named genus, Sinorhizobium, take priority in nomenclature. There is no justification in the International Code of Nomenclature of Bacteria (Prokaryotes) for this step; Ensifer is the correct name of the genus, with Ensifer adhaerens as the type species. Species previously allocated to Sinorhizobium are here proposed as the new combinations Ensifer arboris, Ensifer fredii, Ensifer kostiensis, Ensifer kummerowiae, Ensifer medicae, Ensifer meliloti, Ensifer saheli, Ensifer terangae and Ensifer xinjiangensis. Sinorhizobium morelense was proposed in 2002 [Wang, E. T., Tan, Z. Y., Willems, A., Fernández-López, M., Reinhold-Hurek, B. & Martínez-Romero, E., Int J Syst Evol Microbiol 52, 1687–1693, 2002
], but a consideration of all published data indicate that it is a nitrogen-fixing genomovar and later heterotypic synonym of Ensifer adhaerens. A Request for an Opinion is made as to whether or not the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 is legitimate.
Casida (1982) proposed the binomial Ensifer adhaerens for a bacterium that multiplied by budding and was predatory on other bacteria. At present, Ensifer is recorded as a monotypic genus, with E. adhaerens as the type species. Willems et al. (2003) compared the type strain and one other strain of E. adhaerens, both isolated by Casida, with a selection of strains representing Sinorhizobium species. Methods involved comparisons based on the 16S rDNA sequence and part of the recA sequence, DNA hybridization of nod gene probes, DNA base composition, DNA–DNA reassociation data, SDS-PAGE of whole-cell proteins, auxanographic characteristics, antibiotic sensitivities and nodulation assays. The only datasets in which the type species of Ensifer and Sinorhizobium were included, enabling the differentiation of the two genera, referred to a large part of the 16S rDNA sequence and a part of the sequence of recA. Willems et al. (2003) concluded that Ensifer Casida 1982 and Sinorhizobium Chen et al. 1988 were synonyms, acknowledging Ensifer as the earlier synonym. Elsewhere, Wang et al. (2002) reported a novel species, Sinorhizobium morelense, which shared the budding characteristic and high antibiotic resistance of E. adhaerens. Data reported in these papers confirmed the very close relationship of Ensifer and Sinorhizobium and justify the amalgamation of these two genera.
Willems et al. (2003) requested an Opinion of the Judicial Commission of the International Committee on Systematics of Prokaryotes, with a proposal that the name Sinorhizobium should be preferred to Ensifer, and referred to Rule 38 of the International Code of Nomenclature of Bacteria (Prokaryotes) [‘the Code’ (Lapage et al., 1992)] because they believed that the union of the two genera with Ensifer as the generic name would cause confusion in bacteriology. The reasons given in their request were:
(i) Sinorhizobium is a well-known genus and Ensifer is less well known;
(ii) Sinorhizobium contains nine species while Ensifer contains one species;
(iii) the descriptive name derived from ‘rhizobium’ implies a distinctive feature of the organisms;
(iv) Ensifer was proposed before comparative 16S rDNA sequence analyses allowed phylogenetic inferences to be made. Had such analyses been possible, the close relationship of E. adhaerens to Rhizobium would have been recognized and this species would have been included in Rhizobium.
In making their request, Willems et al. (2003) do not refer correctly to any rule that supports their proposal. The intention of Rule 38 is to emphasize the importance of the rule of priority, covered in detail in Rule 23, and the status of synonymy, covered in Rule 24. Bacterial names are accorded priority in order of publication, and only the Judicial Commission may make a determination that an earlier name is to be conserved over a later name (Rule 23a; Note 4). The Code does not specify the criteria for conservation of a later over an earlier synonym, but indicates that names may be rejected only if they are ambiguous, doubtful, cause confusion, are perplexing or are perilous. Guidance is offered in Rule 55, which states that a legitimate name may not be replaced merely because it is inappropriate or disagreeable, another name is preferable or is better known, or the name no longer describes the organism. The Request for an Opinion of Willems et al. (2003) runs counter to all these criteria.
The argument of Willems et al. (2003) that the availability of comparative 16S rDNA sequence analyses when E. adhaerens was first characterized (Casida, 1982) would have led to its inclusion in Rhizobium is highly doubtful in the absence of the recognition of other Sinorhizobium species before the report of Chen et al. (1988). The budding, predatory organism E. adhaerens might have been recognized as being related to the Agrobacterium–Rhizobium clade, but on the separate (Sinorhizobium) branch. In the absence of demonstrated nitrogen-fixing or gall-forming properties, its allocation to a separate genus was almost certainly assured, following the reasoning of Willems et al. (2003).
Central to the proposal of Willems et al. (2003) is their view that bacterial names should be familiar and descriptive. However:
(i) if names are to take precedence merely because of their familiarity, the formal organization of nomenclature based primarily on priority will be subverted;
(ii) although the generic name Sinorhizobium was published in 1988, the International Committee on Systematic Bacteriology Subcommittee on the Taxonomy of Agrobacterium and Rhizobium did not endorse the name in 1992 (Martinez-Romero & Jarvis, 1993). The name Sinorhizobium came into general use only after 1994 (de Lajudie et al., 1994).
(iii) A recent Request for an Opinion (Logan et al., 1998) that a later synonym be preferred to an earlier synonym merely because it was a more descriptive name was rejected (De Vos & Trüper, 2000; Trüper, 2002). The reasons have also been explained elsewhere (Young, 2000).
Nitrogen-fixing bacteria may represent only a part of the overall diversity in the genera of the Rhizobiaceae. The present record of characterized species is strongly biased in favour of organisms of anthropocentric interest. There is little basis at present for believing even that nitrogen-fixing strains are the predominant populations in species originally identified by their nitrogen-fixing ability. As the catalogue of bacterial diversity is expanded, names based on characteristics such as nitrogen fixation can be expected only to become more confusing. It is misleading to regard names of bacteria as descriptive, and it does no service to bacteriologists when taxonomists support this interpretation.
‘Sinorhizobium adhaerens’ – Request for an Opinion
Willems et al. (2003) proposed that E. adhaerens be renamed as ‘Sinorhizobium adhaerens’.
On the basis that the discussion above accurately reflects the correct nomenclatural relationships of Ensifer and Sinorhizobium, it is proposed here that the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 is illegitimate. E. adhaerens is the legitimate heterotypic earlier synonym (the Code; Rule 23). A decision of the Judicial Commission is sought.
Reclassification of Sinorhizobium species
The inclusion of E. adhaerens and Sinorhizobium species in a single genus requires the recombination of Sinorhizobium species in the genus Ensifer, the name that takes priority. An emended description of the genus Ensifer, combining that of Casida (1989) and that of Sinorhizobium by Kuykendall et al. (2003), is presented. New combinations of Ensifer species are proposed.
Emended description of the genus Ensifer Casida 1982, 339VP
Rods, 0·5–1·0x1·0–3·0 µm. Commonly pleomorphic under adverse growth conditions. Some species multiply by budding. Cells usually contain granules of poly-
-hydroxybutyrate that are refractile under phase-contrast microscopy. Non-spore-forming. Gram-negative. Motile by means of one polar or subpolar flagellum or one to six peritrichous flagella. Fimbriae have been described for a few strains. Aerobic, possessing a respiratory type of metabolism with oxygen as the terminal electron acceptor. The optimum temperature is 25–30 °C, but a wide range of temperatures can be tolerated: most strains can grow at 35 °C, some strains can grow at 10 °C and others grow at temperatures up to 42–44 °C. Tolerate 1·0 % NaCl; some strains grow well on media containing 4·5 % NaCl. The optimum pH is 6–8, but some strains can grow at pH 5·0 and others at pH 10·5. Colonies are circular, convex, semi-translucent, raised and mucilaginous and usually 2–4 mm in diameter within 3–5 days on yeast/mannitol/mineral-salts agar. Generation times are 3–6 h. Chemo-organotrophic, utilizing a wide range of carbohydrates and salts of organic acids as carbon sources, producing acid without gas formation. Cellulose and starch are not utilized. Produce an acidic reaction in mineral-salts medium containing mannitol. Growth on carbohydrate media is often accompanied by copious extracellular polysaccharide slime production. Do not utilize cellulose or starch. Ammonium salts, nitrate, nitrite and most amino acids can serve as nitrogen sources. All strains require pantothenate and nicotinic acid. Peptone is poorly utilized. Casein and agar are not hydrolysed. Strains produce cytochrome oxidase and catalase. 3-Ketolactose is not produced from lactose. Some species are recorded as resistant to a wide variety of antibiotics. Strains of most species identified so far are characteristically able to invade temperate-zone and tropical-zone leguminous plants (family Leguminosae) and to incite the production of root nodules, inside which the bacteria occur as intracellular nitrogen-fixing microsymbionts. In root nodules, the bacteria occur as endophytes exhibiting pleomorphic forms. Strains of nitrogen-fixing isolates exhibit varying degrees of host specificity. Strains of at least one species, the type species, are capable of the predation of other bacteria. The G+C content of the DNA is 57–66 mol% (Tm). The type species is Ensifer adhaerens Casida 1982VP.
Description of Ensifer arboris (Nick et al. 1999) comb. nov.
The description is the same as that given for Sinorhizobium arboris by Nick et al. (1999). The type strain is ATCC BAA-226T=DSM 13375T=HAMBI 1552T=LMG 14919T.
Description of Ensifer fredii (Scholla and Elkan 1984) comb. nov.
The description is the same as that given for Sinorhizobium fredii by Chen et al. (1988). The type strain is ATCC 35423T=CCUG 27877T=DSM 5851T=HAMBI 2075T=ICMP 11139T=IFO 14780T=LMG 6217T=NRRL B-14594T=USDA 205T.
Description of Ensifer kostiensis (Nick et al. 1999) comb. nov.
The description is the same as that given for Sinorhizobium kostiense by Nick et al. (1999). The type strain is ATCC BAA-227T=DSM 13372T=HAMBI 1489T=LMG 19227T.
Description of Ensifer kummerowiae (Wei et al. 2002) comb. nov.
The description is the same as that given for Sinorhizobium kummerowiae by Wei et al. (2002). The type strain is CCBAU 71714T=AS 1.3046T.
Description of Ensifer medicae (Rome et al. 1996) comb. nov.
The description is the same as that given for Sinorhizobium medicae by Rome et al. (1996). The type strain is A 321T=HAMBI 2306T=ICMP 13798T=USDA 1037T.
Description of Ensifer meliloti (Dangeard 1926) comb. nov.
The description is the same as that given for Sinorhizobium meliloti by de Lajudie et al. (1994). The type strain is ATCC 9930T=CCUG 27879T=CFBP 5561T=DSM 30135T=HAMBI 2148T=ICMP 12623T=IFO14782T=LMG 6133T=NCAIM B.01520T=NRRL L-45T=USDA 1002T.
Description of Ensifer saheli (de Lajudie et al. 1994) comb. nov.
The description is the same as that given for Sinorhizobium saheli by de Lajudie et al. (1994). The type strain is ATCC 51690T=DSM 11273T=HAMBI 215T=ICMP 13648T=LMG 7837T=ORS 609T.
Description of Ensifer terangae (de Lajudie et al. 1994) comb. nov.
The description is the same as that given for Sinorhizobium terangae by de Lajudie et al. (1994). The type strain is ATCC 51692T=DSM 11282T=HAMBI 220T=ICMP 13649T=LMG 7834T=ORS 1009T.
Description of Ensifer xinjiangensis (Chen et al. 1988) comb. nov.
The description is the same as that given for Sinorhizobium xinjiangense by Chen et al. (1988). The type strain is ATCC 49357T=CCBAU 110T=DSM 5852T=HAMBI 1673T=ICMP 11141T=LMG 17930T.
Sinorhizobium morelense is a later heterotypic synonym of Ensifer adhaerens
The studies of Wang et al. (2002), in which S. morelense is proposed as a new species, and the studies of Willems et al. (2003), using the methods described above, can be taken to provide a comprehensive polyphasic comparison between E. adhaerens and S. morelense. However, the only unequivocal phenotypic difference recorded between the two species is their reaction in the urease test (Wang et al., 2002; Willems et al., 2003). The distinctive feature claimed for S. morelense, high levels of antibiotic resistance (Wang et al., 2002), is also recorded for E. adhaerens (Willems et al., 2003). The comparative studies of 16S rDNA sequence data show that E. adhaerens and S. morelense have essentially the same (99–100 % rDNA) sequence and that the recA sequence of the type strain of S. morelense is embedded in the E. adhaerens sequence cluster, with the type strain of this species as its nearest neighbour (Willems et al., 2003). A comparative study using SDS-PAGE of total proteins included only E. adhaerens and S. morelense strains. No other strains of Sinorhizobium species were included, there was no numerical analysis of data and inspection gave no indication of differentiation between the two species (Willems et al., 2003). The strains unequivocally characterized as S. morelense lacked a nodulating, and hence a nitrogen-fixing, capacity. DNA–DNA reassociation data (Willems et al., 2003) present a complex picture. S. morelense is represented by two strains with less than 70 % (52 and 66 %) mutual similarity. E. adhaerens is considered to be represented by three genomic groups by Willems et al. (2003). These correspond to genomovars sensu Ursing et al. (1995) and do not merit species rank. The incompleteness of the reassociation matrix makes it difficult to judge the genotypic relationships with certainty. In the absence of more compelling data, it is proposed that S. morelense is a later heterotypic synonym of E. adhaerens. E. adhaerens therefore takes precedence, with ATCC 33212T (=LMG 20216T) as the type strain.
ACKNOWLEDGEMENTS
L. D. Kuykendall kindly permitted inspection of the unpublished chapter on Sinorhizobium for the 2nd edition of Bergey's Manual of Systematic Bacteriology. I am grateful to P. R. Johnston and S. R. Pennycook (Landcare Research, Auckland) and to D. R. W. Watson (Plant Diseases Division, Department of Scientific and Industrial Research, Auckland) (retired) for critically reading the manuscript and for their helpful suggestions.
REFERENCES
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Chen, W. X., Yan, G. H. & Li, J. L. (1988). Numerical taxonomic study of the fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38, 392–397.
Dangeard, P. A. (1926). Récherches sur les tubercles radicaux des Légumineuses. Botaniste (Paris) 16, 1–275.
de Lajudie, P., Willems, A., Pot, B. & 7 other authors (1994). Polyphasic taxonomy of rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov., and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol 44, 715–733.
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Kuykendall, L. D., Hashem, F. M. & Wang, E. T. (2003). Genus Sinorhizobium Chen, Yan & Li 1988, 392VP emend. de Lajudie, Willems, Pot, Dewettinck, Maestrojuan, Neyra, Collins, Dreyfus, Kersters & Gillis 1994, 715VP. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 2. New York: Springer (in press).
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Logan, N. A., Heyndrickx, M., Berkeley, R. C. W. & De Vos, P. (1998). Paenibacillus azotofixans (Seldin et al. 1984) Ash et al. 1995 does not have priority over Paenibacillus durum (Smith and Cato 1974) Collins et al. 1994: request for an opinion. Int J Syst Bacteriol 48, 325–326.
Martinez-Romero, M. E. & Jarvis, B. D. W. (1993). International Committee on Systematic Bacteriology Subcommittee on the Taxonomy of Agrobacterium and Rhizobium. Minutes of the meeting, 10 December 1992, Cancun, Mexico. Int J Syst Bacteriol 43, 622.
Nick, G., de Lajudie, P., Eardly, B. D., Suomalainen, S., Paulin, L., Zhang, X., Gillis, M. & Lindström, K. (1999). Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Bacteriol 49, 1359–1368.
Rome, S., Fernandez, M. P., Brunel, B., Normand, P. & Cleyet-Marel, J.-C. (1996). Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Bacteriol 46, 972–980.
Scholla, M. H. & Elkan, G. H. (1984). Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans. Int J Syst Bacteriol 34, 484–486.
Trüper, H. G. (2003). Paenibacillus durus (Collins et al. 1994, formerly Clostridium durum Smith and Cato 1974) has priority over Paenibacillus azotofixans (Seldin et al. 1984). Opinion 73. Int J Syst Evol Microbiol 53, 931.
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Wang, E. T., Tan, Z. Y., Willems, A., Fernández-López, M., Reinhold-Hurek, B. & Martínez-Romero, E. (2002). Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Microbiol 52, 1687–1693.[Abstract]
Wei, G. H., Wang, E. T., Tan, Z. Y., Zhu, M. E & Chen, W. X. (2002). Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigoferae spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52, 2231–2239.[Abstract]
Willems, A., Fernández-López, M., Muñoz-Adelantado, E., Goris, J., De Vos, P., Martínez-Romero, E., Toro, N. & Gillis, M. (2003). Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an Opinion. Int J Syst Evol Microbiol 53, 1207–1217.
Young, J. M. (2000). Suggestions for avoiding on-going confusion from the Bacteriological Code. Int J Syst Evol Microbiol 50, 1687–1689.[Medline]
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