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Taxonomic Note |
1 Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
2 École Nationale Vétérinaire, 23 chemin des Capelles, B.P. 87614, 31076 Toulouse cedex 3, France
3 Veterinary Biomedical Sciences, Royal (Dick) School of Veterinary Studies, Summerhall, Edinburgh EH9 1QH, UK
4 Department of Microbiology, King's College London Dental Institute at Guy's, King's College and St Thomas' Hospitals, Floor 28 Guy's Tower, Guy's Campus, London SE1 9RT, UK
Correspondence
Donovan P. Kelly
D.P.Kelly{at}warwick.ac.uk
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) with Paracoccus denitrificans as the type species. The type strain ATCC 17741T was originally isolated from soil by Martinus Beijerinck, using enrichment culture on tartrate and nitrate, and called ‘Micrococcus denitrificans’ (Beijerinck & Minkman, 1910). In the original paper, no further description was given of the species, and the organism was not archived by the Delft collection (as LMD 22.21T, now known as NCCB 22021T) until 1922. No description of ‘M. denitrificans’ appeared in early editions of Bergey's Manual of Determinative Bacteriology (e.g. the first edition of 1923 or the fifth edition of 1939). ‘M. denitrificans’ was cited in the sixth edition, but only as one of a number of species ‘listed here chiefly for their historical interest’ (Breed et al., 1948), and the first full description of ‘M. denitrificans’ appeared only in the seventh edition (Breed et al., 1957). For many years, P. denitrificans remained the only authentic species of Paracoccus, with the result that biotypes actually differing from each other at the species level were assigned to this species (Baj, 2000; Dobson & Franzmann, 1996; Kelly et al., 2000; Jordan et al., 1997; Nokhal & Schlegel, 1983; Van Verseveld & Stouthamer, 1992). An example was Thiosphaera pantotropha (strain GB17T=ATCC 35512T), which was transferred to P. denitrificans on the basis of showing 100 % 16S rRNA gene sequence identity to a supposed example of the type strain of P. denitrificans (LMG 4218; Ludwig et al., 1993; Robertson & Kuenen, 1983). Moreover, another putative example of the type strain of P. denitrificans (DSM 65) showed 85 % DNA–DNA hybridization with T. pantotropha GB17T. Subsequently, additional species of Paracoccus were described, with 14 being recognized by Kelly et al. (2000), and 24 are now recognized in the literature (Table 1), although not all these names are validly published.
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, who showed by analysis of protein profiles and c-type cytochromes that some strains of [P. denitrificans] were likely to be of a different species. These included a supposed derivative of the type strain held in the Ghent collection (LMG 4218), the original T. pantotropha isolate (GB17T) and DSM 65. Goodhew et al. (1996) were the first to suggest that a separate species, with GB17T as the type strain, might be necessary to describe some of the extant strains of P. denitrificans. A comprehensive study by Rainey et al. (1999), using 16S rRNA gene sequence comparisons and DNA–DNA hybridization among culture collection strains of P. denitrificans, confirmed the findings of Goodhew et al. (1996) and confirmed the creation of a novel species, Paracoccus pantotrophus, with the former T. pantotropha strain GB17T as the type strain. The definitive study of Rainey et al. (1999) resulted in numerous other culture collection strains previously regarded as representative of P. denitrificans, including LMG 4218, being redesignated strains of P. pantotrophus (Table 2).
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) recognizes the establishment of P. pantotrophus, but unfortunately perpetuates the incorrect assignment of a number of its strains to P. denitrificans. Microbiologists using this chapter of the second edition of Bergey's Manual of Systematic Bacteriology (Van Spanning et al., 2005) to assist in taxonomic assignments should note a number of amendments, which are listed below. These are provided in the spirit of the request made by Bergey et al. (1923) in the first edition of Bergey's Manual of Determinative Bacteriology that ‘the assistance of all bacteriologists is earnestly solicited in the correction of possible errors in the text’. 1. The entry for P. denitrificans cites the type strain as being represented by ATCC 17741, DSM 65, DSM 413, LMD 22.21 and LMG 4218. Of these, DSM 65 and LMG 4218 are strains of P. pantotrophus. LMD 22.21 is now known as NCCB 22021.
2. The entry for P. denitrificans cites the GenBank 16S rRNA gene sequence accession numbers for the ‘type strain’ as Y16927 (ATCC 17741), Y16935 (DSM 65), D13480 (IAM 12479), Y16928 (LMD 22.21, now known as NCCB 22021) and X69159 (LMG 4218). Of these, D13480, Y16935 and X69159 are sequences for P. pantotrophus, with X69159 also being 100 % identical to the sequence from the type strain of P. pantotrophus (LMD 82.5T, now known as NCCB 82005T; Ludwig et al., 1993).
3. The entry for P. pantotrophus should be expanded to include DSM 65 and LMG 4218 as valid examples of the type strain and the accession number for the 16S rRNA gene sequence of the type strain (ATCC 35512T) needs to be cited (Y16933).
4. There are inconsistencies between the tabulated and text information given by Van Spanning et al. (2005), resulting in uncertainty about some key properties of several species. It needs to be clear that P. denitrificans, P. pantotrophus and Paracoccus versutus can all grow chemolithoautotrophically with thiosulfate as the sole energy source (Kelly & Harrison, 1989; Kelly et al., 2000; Robertson & Kuenen, 1983; Sijderius, 1946; Taylor & Hoare, 1969) and that P. versutus is capable of growth on methanol as the sole energy source (Kelly & Wood, 1982; Kelly et al., 2000; Taylor & Hoare, 1969). Moreover, the ability to grow on carbon disulfide is a property of P. pantotrophus, not yet shown also to apply to P. denitrificans (Jordan et al., 1995, 1997; Rainey et al., 1999).
Comparison of 16S rRNA gene sequences is routinely used to ensure the correct placement of strains of Paracoccus within the alpha-3 subgroup of the class Alphaproteobacteria. The class itself is delimited by the 16S rRNA relationships of its members (Kainth & Gupta, 2005) with DNA–DNA relatedness and structural and physiological properties being applied as supporting diagnostic features at the species level. It is notable that relatively few separate isolations of P. denitrificans have been reported since the first publication by Beijerinck & Minkman (1910): the valid strains in culture collections seem to have been derived either from the original isolate or from those isolated by Verhoeven et al. (1954) (DSM 413T) and Vogt (1965) (DSM 415) and more recently by Ruff et al. (2003) (DSM 15418).
Inevitably, international culture collections do not always cite the correct type strains in their catalogues. As shown by Goodhew et al. (1996), the culture history of a strain as reported by a culture collection does not always correspond to the correct identity of that strain. For example, the culture history of the Ghent strain of P. pantotrophus, LMG 4218, was supposedly Beijerinck (1909) 
LMD 22.21 (1922) Van Niel Stanier 381 ATCC 17741T LMG 4218. As LMG 4218 is not an example of the type strain of P. denitrificans, it is clear that the culture archived by LMG was incorrect. Also in question is P. denitrificans strain NBRC 16712 (http://www.nbrc.nite.go.jp/e/index.html), whose accession history is given as Van Niel Stanier 381 ATCC 17741T IAM 12479 IFO 16712T NBRC 16712T, where IAM 12479 is now known to be an example of P. pantotrophus. NBRC 16712 is thus a strain for which 16S rRNA gene sequencing is desirable. In Table 2
, we have listed those strains that are correctly assigned to P. denitrificans and those strains that can with reasonable certainty be designated P. pantotrophus. The lists are incomplete as some strains not included by us but listed as P. denitrificans in culture collections are probably derived from the original type culture (although their culture history is not necessarily clear). There is a case, however, for further study of any strains not yet subjected to 16S rRNA gene sequencing, in order to confirm their phylogenetic relationships.
An example of the kind of assessment we recommend has been provided to us by the DSMZ. Eleven strains catalogued by the DSMZ as P. denitrificans have been subjected to diagnostic sequencing of their 16S RNA genes (E. Stackebrandt and J. Swiderski, personal communications). Three of these, DSM 413T, DSM 415 and DSM 15418, were confirmed to show 100 % sequence identity to each other and to the type strain ATCC 17741T, but the remaining eight required reconsideration of their identity.
The 16S rRNA gene sequences of DSM 1403, DSM 1404, DSM 1405, DSM 1406, DSM 6610 and DSM 6392 were identical to each other and showed 100 % identity to that of P. pantotrophus LMG 4218 (and hence 100 % identity to strains ATCC 35512T, DSM 65, NCCB 82005T, JCM 6892 and IAM 12479). DSM 1403, DSM 1405 and DSM 1406 showed 81–98 % DNA–DNA hybridization with DSM 1404, but all four showed a mean of only about 55 % hybridization with two reference strains of P. denitrificans (Stanier 381 and DSM 413T; Auling et al., 1980). Unlike P. denitrificans, the type strain of P. pantotrophus cannot use methanol as a carbon and energy source (Mox–), although it can mutate spontaneously to a Mox+ phenotype (Robertson & Kuenen, 1983; Egert et al., 1993). In common with wild-type P. pantotrophus, DSM 1403, DSM 1404 and DSM 1405 could not grow on methanol, although DSM 1406 was Mox+ (Nokhal & Schlegel, 1983). Strains DSM 1403, DSM 1404, DSM 1405, DSM 1406, DSM 6610 and DSM 6392 must therefore be reassigned to P. pantotrophus.
Strain DSM 1407 was previously found not to cluster with DSM 1403, DSM 1404, DSM 1405, DSM 1406 and DSM 1408 in the computer-based analysis of their properties, and it was also unable to grow on methanol (Nokhal & Schlegel, 1983). DSM 1407 was found by the DSMZ to show 16S rRNA gene sequence identity of 100 % to Paracoccus sp. strain WB1 (GenBank accession no. AF526892) and 98.4 % to P. denitrificans ATCC 17741T, but only 96.2 % 16S rRNA gene sequence identity to P. pantotrophus ATCC 35512T. A BLASTN analysis of the sequence from Paracoccus sp. strain WB1 showed it to be most similar to 12 strains of P. pantotrophus (with 98.3 % identity to the type strain), with 97.1–97.8 % identity to strains of P. denitrificans, P. versutus, ‘Paracoccus thiophilus’ and ‘Paracoccus bengalensis’. DNA–DNA hybridization analysis by Auling et al. (1980) found strain DSM 1407 to show only 53–61 % relatedness with P. pantotrophus DSM 1404 and two reference strains of P. denitrificans. Strain DSM 1407 can thus not be assigned to either P. pantotrophus or P. denitrificans on the basis of the data currently available and may represent a novel species.
Strain DSM 1408 (strain N11 of Nokhal & Schlegel, 1983) proved more problematic, as its 16S rRNA gene sequence showed highest identities to those of Paracoccus sp. strain R-24616 (100 %; GenBank accession no. AM084041) and Paracoccus alcaliphilus JCM 7364T (98.2 %; D32238). The sequence from strain R-24616 showed only 97.5–97.6 % identity to those of P. alcaliphilus JCM 7364T, P. denitrificans ATCC 17741T and Paracoccus aminophilus ATCC 49673T (GenBank accession no. AY014176). Strain DSM 1408 is thus unlikely to be a strain of P. denitrificans and is also unlikely to belong to either P. alcaliphilus or P. aminophilus, as neither of these can denitrify (Urakami et al., 1989, 1990) and the pH range for growth of DSM 1408 is pH 6.0–8.0, compared with pH 7.0–9.5 for P. alcaliphilus (Urakami et al., 1989). Like P. pantotrophus and P. aminophilus, DSM 1408 cannot grow on methanol (Nokhal & Schlegel, 1983; Urakami et al., 1990). It seems that DSM 1408 cannot be assigned unequivocally to any currently recognized species of Paracoccus, and it was also found to be different from DSM 1403, DSM 1404, DSM 1405, DSM 1406 and DSM 1407 in the systematic analysis of Nokhal & Schlegel (1983). With strains R-24615, R-24616, R-24617 and R-25058 (based on the 16S rRNA gene sequences available from GenBank), DSM 1408 appears to represent a novel clade within the genus, clearly meriting further study.
It has been our aim in this note to clarify the taxonomic status of the numerous culture collection strains of two key species of Paracoccus that have been used for many years in fundamental biochemical studies and as reference species in the identification of new isolates of Paracoccus. It is important to the integrity of taxonomy that any confusion about the identity of strains of the type species should be clarified.
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ACKNOWLEDGEMENTS |
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