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Int J Syst Evol Microbiol 53 (2003), 1439-1443; DOI  10.1099/ijs.0.02526-0
© 2003 International Union of Microbiological Societies

Reclassification of Desulfotomaculum auripigmentum as Desulfosporosinus auripigmenti corrig., comb. nov.

Erko Stackebrandt, Peter Schumann, Esther Schüler and Hans Hippe

DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, 38124 Braunschweig, Germany

Correspondence
Erko Stackebrandt
Erko{at}DSMZ.de


   ABSTRACT
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The species Desulfotomaculum auripigmentum is reclassified as Desulfosporosinus auripigmenti corrig., comb. nov. on the basis of morphological and physiological traits, phylogenetic position and chemotaxonomic properties. Characteristics supplementary to those provided in the original description reveal that the type strain, DSM 13351T (=ATCC 700205T), forms oval, subterminal to terminal spores, possesses LL-diaminopimelic acid and contains MK-7 as the predominant menaquinone, while the whole-cell methanolysate contains even-carbon, straight-chain saturated and mono-unsaturated fatty acids and 1,1-dimethylacetals as major components. DNA–DNA reassociation values below 30 % for Desulfosporosinus orientis DSM 765T and Desulfosporosinus meridiei DSM 13257T demonstrate that strain DSM 13351T shows sufficient genomic differences to maintain its species status. Lack of motility, a smaller cell diameter and the ability to use malate and glycerol as electron donors and fumarate and arsenate as electron acceptors are the main properties that differentiate Desulfosporosinus auripigmenti from the other two species of the genus.

Published online ahead of print on 21 February 2003 as DOI 10.1099/ijs.0.02526-0.

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Desulfosporosinus auripigmenti DSM 13351T and Desulfosporosinus orientis DSM 7493 are AJ493051 and AJ493052, respectively.


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The species Desulfotomaculum auripigmentum, type strain ATCC 700205T (=DSM 13351T) (Newman et al., 1997Go), was affiliated with Desulfotomaculum mainly on the basis of 16S rDNA analysis. This non-motile, sausage-shaped, arsenate- and sulfate-reducing Gram-positively staining bacterium, for which spore formation had not been reported, was placed as a phylogenetic neighbour of Desulfotomaculum orientis in the 16S rDNA dendrogram of relationships (96·2 % similarity). However, in the same year in which Desulfotomaculum auripigmentum was described, Desulfotomaculum orientis was reclassified as the type species of a new genus, namely Desulfosporosinus, as Desulfosporosinus orientis (Stackebrandt et al., 1997Go). As the publication processes overlapped each other, none of the two research groups was aware of the other group's work. In 2001, a second species of the genus Desulfosporosinus, Desulfosporosinus meridiei (type strain DSM 13257T), was described (Robertson et al., 2001Go) which branched phylogenetically adjacent to Desulfotomaculum auripigmentum DSM 13351T (97·6 % 16S rRNA gene sequence similarity), while the sequence similarity to Desulfosporosinus orientis DSM 765T was slightly lower (96·7 %). Despite the grouping of a Desulfotomaculum species between two Desulfosporosinus species, the generic affiliation of Desulfotomaculum auripigmentum remained unchallenged.

As the 16S rRNA gene sequence of the type strain of Desulfotomaculum auripigmentum, ATCC 700205T, comprised only 1263 nt (GenBank accession no. U85624), the sequence analysis of strain DSM 13351T was repeated (AJ493051), using the method described by Rainey et al. (1996)Go, and the phylogenetic position was reassessed by applying the treeing algorithm of De Soete (1983)Go. Using the new sequence comprising 1532 bases, Desulfotomaculum auripigmentum was found to share 97·4 and 97·9 % similarity with Desulfosporosinus orientis DSM 765T and Desulfosporosinus meridiei, respectively. Desulfosporosinus orientis DSM 7439, the 16S rRNA gene sequence of which was also determined in this study (GenBank accession no. AJ493052), was highly related to the type strain DSM 765T (99·5 %), while strain DSM 8344 was significantly less closely related to DSM 765T (96·2 %) (Stackebrandt et al., 1997Go; Robertson et al., 2001Go). Strain DSM 8344 showed 97·6 % similarity to the type strains of Desulfotomaculum auripigmentum and Desulfosporosinus meridiei. All these strains formed a coherent phylogenetic cluster that formed a sister lineage to the Desulfitobacterium lineage (93·1–94·4 % similarity) (Fig. 1Go). Members of the genus Desulfotomaculum, described as being phylogenetically heterogeneous and forming three major clusters (Stackebrandt et al., 1997Go), were less than 90 % similar to members of the two lineages embracing the genera Desulfosporosinus and Desulfitobacterium.



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  		Fig. 1. Dendrogram of 16S rRNA gene sequence relationships (De Soete, 1983Go), displaying the phylogenetic position of Desulfotomaculum auripigmentum DSM 13351T, reclassified as Desulfosporosinus auripigmenti in this study. Numbers at branching points refer to bootstrap values (1000 resamplings). Bar, 2 nucleotide substitutions per 100 sequence positions. The tree was rooted with the 16S rRNA gene sequences of Desulfotomaculum species.

 
The phylogenetic clustering of Desulfotomaculum auripigmentum with members of the genus Desulfosporosinus raises the question of whether this species should be reclassified as a species of the genus Desulfosporosinus. The 16S rRNA gene sequences of Desulfosporosinus strains and Desulfotomaculum auripigmentum contain several exclusive signature nucleotides, which clearly distinguish these organisms from members of the genus Desulfitobacterium (Table 1Go). The respective nucleotides of Desulfotomaculum species are not listed because the species do not constitute a phylogenetically coherent taxon. Members of the genus Desulfosporosinus, as well as Desulfotomaculum auripigmentum, possess LL-diaminopimelic acid as the diagnostic amino acid of peptidoglycan, as determined by the methods of Schleifer & Kandler (1972)Go. However, LL-diaminopimelic acid also occurs in some members of the genus Desulfotomaculum, for example, Desulfotomaculum thermoacetoxidans DSM 5813T and Desulfotomaculum thermobenzoicum subsp. thermobenzoicum DSM 6193T, and in species of the genus Desulfitobacterium [Desulfitobacterium dehalogenans DSM 9161T, Desulfitobacterium hafniense DSM 10664T, as well as in Desulfitobacterium sp. strain PCE1 (Gerritse et al., 1992Go)], whereas Desulfotomaculum aeronauticum DSM 10349T, Desulfotomaculum geothermicum DSM 3669T and Desulfotomaculum nigrificans DSM 574T contained meso-diaminopimelic acid (result of this study, except for strain PCE1). Thus, this property is not exclusive taxonomically.


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  		Table 1. Oligonucleotide signatures distinguishing members of the genus Desulfosporosinus and Desulfotomaculum auripigmentum from members of the genus Desulfitobacterium

 
To verify the species status of the two Desulfosporosinus species and of Desulfotomaculum auripigmentum, DNA–DNA pairing studies were performed between the type strains. DNA was isolated by chromatography on hydroxylapatite by the procedure of Cashion et al. (1977)Go. DNA–DNA hybridization was carried out in 2xSSC at 65 °C according to De Ley et al. (1970)Go, using a Gilford System 2600 spectrophotometer (Gilford Instrument Laboratories) equipped with a Gilford 2527-R thermoprogrammer and plotter. While Desulfosporosinus orientis DSM 765T shared 54 % DNA binding with Desulfosporosinus meridiei DSM 13257T, the DNA similarity of these type strains to Desulfotomaculum auripigmentum DSM 13351T was 30 and 29 %, respectively. DNA–DNA similarity values below 55 % correlated with the moderate 16S rRNA gene sequence similarities and confirmed that each of the three species are genomically distinct taxa. This is also reflected by different EcoRI riboprint patterns (Fig. 2Go) generated by the RiboPrinter (a microbial characterization system; DuPont Qualicon) according to Bruce (1996)Go.



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  		Fig. 2. Riboprint patterns of Desulfosporosinus strains and Desulfosporosinus auripigmenti DSM 13351T, generated with EcoRI. Lanes: 1, Desulfosporosinus meridiei DSM 13257T; 2, Desulfosporosinus auripigmenti DSM 13351T; 3, Desulfosporosinus sp. DSM 8344; 4, Desulfosporosinus orientis DSM 765T; 5, Desulfosporosinus orientis DSM 7439.

 
In contrast to the type strains of Desulfosporosinus orientis and Desulfosporosinus meridiei, Desulfotomaculum auripigmentum DSM 13551T is not motile, and spores had not been observed. In this respect, strain DSM 13551T also differs from the genus description of Desulfotomaculum (Campbell & Singleton, 1986Go), reported to embrace spore-forming and motile organisms. To determine whether Desulfotomaculum auripigmentum does in fact fail to produce spores, strain DSM 13551T was grown in DSMZ medium no. 641 (Deutsche Sammlung von Mikroorganismen und Zellkulturen Catalogue of Strains, 2001, 7th edn), containing 2·5 g lactate l-1, at 28 °C for 4 days. Subterminal to terminal ellipsoid spores were formed in some cells (Fig. 3Go). The same medium was used for obtaining information on chemotaxonomic properties lacking in the original description of Desulfotomaculum auripigmentum, i.e. isoprenoid quinones (Collins et al., 1977Go; Groth et al., 1996Go) and cellular fatty acids (Miller, 1982Go; Sasser, 1990Go). MK-7 was the principal quinone (57 %), while MK-5 (40 %) and MK-6 (3 %) were the minor quinones. The major fatty acids (>5 % of the total) were even-carbon, straight-chain saturated and mono-unsaturated fatty acids. 1,1-Dimethylacetals and traces of aldehydes, branched-chain fatty acids and cyclopropane fatty acids occur as well (see species description for the percentage of total values). The fatty acid composition differs from that described for Desulfosporosinus meridiei (Robertson et al., 2000Go) in the lack of substantial amounts of iso- and anteiso-branched-chain fatty acids (2·5 versus 29 %) but confirms the fatty acid composition given in the emended genus description, in which it is stated that members of the genus Desulfosporosinus contain minor amounts of branched-chain fatty acids (Robertson et al., 2001Go) or even no branched-chain fatty acid (Stackebrandt et al., 1997Go). We therefore propose, on the basis of the phylogenetic position, common chemotaxonomic properties, sulfate reduction and incomplete oxidation of organic compounds (Table 2Go), to reclassify Desulfotomaculum auripigmentum as Desulfosporosinus auripigmenti corrig., comb. nov. (auripigmentum, a noun in apposition, has been changed to auripigmenti, the genitive noun). Lack of motility, a smaller cell diameter and the ability to use malate and glycerol as electron donors and fumarate and arsenate as electron acceptors differentiate this species from the other two species of the genus Desulfosporosinus. This transfer demands the emendation of the genus description of Desulfosporosinus.



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  		Fig. 3. Phase-contrast micrograph of spore-forming and non-spore-forming cells of Desulfosporosinus auripigmenti. Bar, 10 µm.

 

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  		Table 2. Some biochemical and chemotaxonomic characteristics of species of the genus Desulfosporosinus, including the reclassified species Desulfosporosinus auripigmenti

ND, Not determined. All of the species share the following properties: LL-diaminopimelic acid is present in the peptidoglycan; oxidation of hydrogen with carbon dioxide; sulfate, thiosulfate and sulfite are used as electron acceptors in the presence of lactate; incomplete oxidation.

 
Emended description of the genus Desulfosporosinus (Stackebrandt et al. 1997Go, Robertson et al. 2001Go, emend.)
Desulfosporosinus [De.sul.fo.spo.ro.si'nus. L. pref. de from; L. n. sulfur sulfur; M.L. n. spora spore; L. n. sinus bend; N.L. masc. n. Desulfosporosinus a spore-forming curved (organism) that reduces sulfur compounds].

Gram-negative rods that have a multi-layered cell wall structure. Endospores present, oval and subterminal to (almost) terminal, causing the cells to swell slightly. Non-motile or motile with lateral or peritrichous flagella. Strictly anaerobic. If determined, desulfoviridin and cytochrome c3 absent and bisulfite reductase P582 present. Sulfate and thiosulfate are reduced to sulfide in the presence of lactate but not in the presence of acetate or fructose. Incomplete oxidation of organic compounds to acetate. Acetate is the fermentation end-product; capable of homoacetogenic growth. Grows autotrophically with hydrogen plus sulfate. LL-Diaminopimelic acid is the diagnostic diamino acid of peptidoglycan. Contains menaquinone with a side-chain with seven isoprene units (MK-7 type). Predominant fatty acids are even-numbered, saturated and unsaturated fatty acids; significant amounts of 1,1-dimethylacetals have been found in Desulfosporosinus auripigmenti; traces of iso- and anteiso-branched-chain fatty acids and cyclopropane fatty acids may occur. The G+C content of the DNA is 41·6–45·9 mol%. Phylogenetically, a member of the Clostridium–Bacillus subphylum of Gram-positive bacteria.

The type species is Desulfosporosinus orientis.

Description of Desulfosporosinus auripigmenti corrig., comb. nov.
Basonym Desulfotomaculum auripigmentum (Newman et al. 1997Go). Desulfosporosinus auripigmenti [au.ri.pig.men'ti. L. neut. n. aurum gold; L. neut. n. pigmentum colour, pigment; N.L. gen. n. auripigmenti of golden pigment, referring to the colour of precipitate (arsenosulfide, As2S3) which is formed after reduction of arsenate and sulfate].

Phylogenetic and chemotaxonomic data indicate that Desulfotomaculum auripigmentum is more closely related to species of Desulfosporosinus than to any species of Desulfotomaculum. The cultural, morphological and physiological description of the species, given by Newman et al. (1997)Go, is unchanged. In addition to the original description, cells occasionally form oval, subterminal to terminal spores. The diagnostic amino acid of peptidoglycan is LL-diaminopimelic acid; MK-7 is the predominant isoprenoid quinone; MK-5 and MK-6 are minor components. The major fatty acids (>5 %) are (as percentages of the total) 16 : 1cis9 (31·6 %), 16 : 0 (14·2 %), 16 : 0-dimethylacetal (13·4 %), 18 : 1cis9 (7·5 %) and 18 : 1cis9-dimethylacetal (7·7 %). Smaller amounts (1–5 %) of the following fatty acids are present (percentages of the total are shown in parentheses): 18 : 0 (2·8 %), 14 : 0 (2·2 %), 16 : 0-aldehyde (1·9 %), 16 : 1cis7 (1·5 %), 16 : 1 cis9-dimethylacetal (1·7 %), 17 : 1cis8 (1·3 %), 17 : 1cis9 (1·1 %), 18 : 1cis11 (2·5 %), 18 : 1cis13 (1·0 %), 18 : 0-dimethylacetal (2·0 %) and 18 : 1cis11-dimethylacetal (4·4 %). Minor amounts of cyclo 17 : 0 (0·6 %) are present. The G+C content of the DNA is 41·6 mol%.

The type strain is DSM 13351T (=ATCC 700205T).


   ACKNOWLEDGEMENTS
 
The technical assistance of Bettina Sträubler (DNA reassociation), M. Jando (fatty acid analysis) and Anika Vester (chemotaxonomy) is highly appreciated. We thank Stefan Spring for constructive criticism.


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Groth, I., Schumann, P., Weiss, N., Martin, K. & Rainey, F. A. (1996). Agrococcus jenensis gen. nov., sp. nov., a new genus of actinomycetes with diaminobutyric acid in the cell wall. Int J Syst Bacteriol 46, 234–239.[Abstract/Free Full Text]

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