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Taxonomic Note |
1 Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
2 NITE Biological Research Center, National Institute of Technology and Evaluation, 2-5-8 Kazasakamatari, Kisarazu-shi, Chiba, 292-0818 Japan
3 Lehrstuhl für Mikrobiologie und Archaeenzentrum, Universität Regensburg, Universitätsstraße 31, 93053 Regensburg, Germany
4 Centro de Biología Molecular (CSIC-UAM), Universidad Autónoma de Madrid, Cantoblanco, 28049 Madrid, Spain
5 Department of Microbiology, King's College London, Dental Institute, 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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to accommodate four former Thiobacillus species. At that time, Moreira & Amils (1997) renamed ‘Thiobacillus cuprinus’ as Thiomonas cuprina comb. nov., but the name ‘Thiobacillus cuprinus’ had never been validly published (Associate Editor, IJSB, 1997), so, while the name ‘Thiobacillus cuprinus’ remains the basonym for the species, the new name should be attributed to Moreira and Amils as Thiomonas cuprina sp. nov. The four new species names proposed by Moreira & Amils (1997) were Thiomonas cuprina, Thiomonas intermedia, Thiomonas perometabolis and Thiomonas thermosulfata. Subsequently, two further species were assigned to the genus: Thiomonas delicata and ‘Thiomonas arsenivorans’ (Kelly & Wood, 2005; Katayama et al., 2006; Battaglia-Brunet et al., 2006). We have shown that Thiomonas delicata and ‘Thiomonas arsenivorans’ share >99 % 16S rRNA gene sequence identity (Katayama et al., 2006), indicating a very close phylogenetic relationship. We also previously suggested that Thiomonas cuprina should be considered for reassignment to a new genus, as its published 16S rRNA gene sequence showed only 85–89 % identity to that of any other Thiomonas species (Katayama et al., 2006). We have now carried out a reanalysis of the 16S rRNA gene sequence of Thiomonas cuprina strains, and extended the comparison of the 16S rRNA genes of strains of Thiomonas cuprina, Thiomonas delicata and ‘Thiomonas arsenivorans’, in order to clarify the interrelationships of these three species.
First, the 16S rRNA gene sequence (1456 bp) of Thiomonas cuprina has been determined for the type strain held by the DSMZ since 1990 (DSM 5495T =NBRC 102145T), and for the original strain (Hö5) after maintenance as a frozen stock culture for 23 years in the University of Regensburg (=NBRC 102094). The sequences were identical to each other, but differed significantly from the previously published sequence for Thiomonas cuprina DSM 5495T (GenBank accession no. U67162). Indeed, it transpires that the sequences for strains of Thiomonas cuprina, Thiomonas delicata and ‘Thiomonas arsenivorans’ differ from each other by only three nucleotides in 1455–1456 nucleotides of sequence. By 16S rRNA gene sequences alone, these three species were therefore indistinguishable.
Consequently, the 16S rRNA gene sequence published by Moreira & Amils (1997) must be discounted: the DNA analysed at that time must have arisen from an organism that was not the type strain of Thiomonas cuprina. The U67162 sequence is in fact rather remote from any other proteobacterial sequence on the databases (Y. Uchino, unpublished data), and rediscovery of the organism from which it came would clearly be of interest. Unfortunately, our new finding also means that the published data on the 5S and 23S rRNA gene sequences of the DNA of the organism studied by Moreira et al. (1994) and Moreira & Amils (1997), as well as reports on the genomic organization and chromosome size, must be treated with caution and merit further investigation (Moreira et al., 1994; Moreira & Amils, 1996, 1997; Marin et al., 1997). The 23S rRNA gene of Thiomonas cuprina DSM 5495T was sequenced independently by Ludwig et al. (1995), using cells provided directly from Regensburg by Karl O. Stetter. This sequence (GenBank accession no. X87292; 2877 nucleotides) shows only 96.9 % identity (2788/2877 aligned bases) to that published by Moreira et al. (1994) (GenBank accession no. X75567; 2858 nucleotides). The 90 mismatches include 51 gaps in the sequence alignment. When the X87292 sequence is run in a BLASTN search (Altschul et al., 1997), the nearest matched sequence is, however, X75567, with the next closest hits being to the complete genomes of Methylibium petroleiphilum PM1T (GenBank accession no. CP000555; 91 % to an unnamed region) and Acidovorax sp. JS42 (CP000539; 89 % to the 23S rRNA gene). The 5S rRNA gene of their strain was also sequenced by Moreira & Amils (1997) (GenBank accession no. U67161), and shows 91.2 % identity to those of Thiomonas intermedia ATCC 15466T (M11538) and Thiomonas perometabolis ATCC 23370T (M11539), but also 97.4 % identity to that of Leptothrix discophora strain Stokes (M35569), so must be viewed with some reservation until it can be re-evaluated.
The species description of Thiomonas cuprina requires only minor amendment, as the properties described have been confirmed as those of the strain from which the correct 16S rRNA gene sequences came (Huber & Stetter, 1990). Emendations to the species description include a listing of the current holdings of the type strain, the citation of the accession numbers for its 16S rRNA gene sequence and the omission of the previously published 5S and 23S rRNA gene sequence accession numbers, until these can be re-evaluated.
Given the virtually identical 16S rRNA gene sequences of Thiomonas cuprina, Thiomonas delicata and ‘Thiomonas arsenivorans’, we have summarized the physiological evidence to retain Thiomonas cuprina and Thiomonas delicata as separate species. Six species of Thiomonas have been described (Kelly & Wood, 2005; Battaglia-Brunet et al., 2006; Katayama et al., 2006): some comparative properties are summarized in Table 1. Thiomonas intermedia (the type species of the genus) and Thiomonas perometabolis share 99.7 % 16S rRNA gene sequence identity (1376/1380 aligned nucleotides) and 100 % identity (116/116 nucleotides) of their 5S rRNA gene sequences, but are recognized as distinct species, both physiologically and by DNA hybridization (Katayama-Fujimura et al., 1983). Thiomonas cuprina shows significant physiological differences from other Thiomonas species, including its ability to oxidize and grow on some metal sulfides (including chalcopyrite, with the release of copper, and arsenopyrite) and its inability to oxidize thiosulfate or tetrathionate (Huber & Stetter, 1990). Moreira & Amils (1997) incorrectly described Thiomonas cuprina as not growing on sulfide minerals (which it can do), but as being able to grow on pyrite (which it cannot). No other Thiomonas species have been reported to grow on chalcopyrite or arsenopyrite, and none can use pyrite as a growth substrate. The supposed ability to grow on pyrite was unfortunately carried over into the chapter on Thiomonas in the latest edition of Bergey's Manual of Systematic Bacteriology (Kelly & Wood, 2005), and is corrected in the amended species description provided below. The ability to grow on thiosulfate or tetrathionate was reported incorrectly as a genus-wide property in the genus description provided by Moreira & Amils (1997), but was corrected by Kelly & Wood (2005). Ferrous iron [Fe(II)] is also oxidized by some Thiomonas species, including Thiomonas delicata (K. B. Hallberg, personal communication), but not by Thiomonas cuprina (Huber & Stetter, 1990; Kelly & Wood, 2005; Battaglia-Brunet et al., 2006; Katayama et al., 2006). Most strains of Thiomonas show optimum growth under mixotrophic conditions, with reduced sulfur compounds and organic supplements (Moreira & Amils, 1997), although one strain has been reported as non-mixotrophic (Pol et al., 2007), and the facultative Thiomonas cuprina can grow rapidly on yeast extract as its sole substrate (µ=0.17–0.23 h–1; Huber & Stetter, 1990).
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). Such metal-rich habitats may thus support a diversity of closely related strains with a range of physiological properties, as was noted for the five strains of Thiomonas cuprina studied originally (Huber & Stetter, 1990).
An emended description of Thiomonas cuprina is given below. The genus description of Thiomonas also requires amendment, as the literature review for the description published in Bergey's Manual of Systematic Bacteriology (Kelly & Wood, 2005) only included published material available up to September 2000. Since then, the ability of some strains to oxidize Fe(II) and arsenite [As(III)] has been proved (Battaglia-Brunet et al., 2002, 2006; Bruneel et al., 2003; Johnson & Hallberg, 2005; Table 1
), and other Thiomonas strains have been shown to oxidize and grow on carbon disulfide, dimethylsulfide and dimethyldisulfide (Pol et al., 2007). The biotechnological application of Thiomonas strains for deodorization and bioremediation have also been recognized (Battaglia-Brunet et al., 2003; Chen et al., 2004; Pol et al., 2007). Most strains show facultative chemolithoautotrophy and chemo-organotrophy, with optimum growth under mixotrophic conditions, but the autotrophic carbon-disulfide-oxidizing strain WZW appeared not to be facultatively chemo-organotrophic or mixotrophic (Pol et al., 2007).
Emended description of Thiomonas Moreira and Amils 1997
Gram-negative, non-spore-forming, short rods that are about 0.3–0.9 µm wide and 1–4 µm long. Cells of most species are motile by means of a single polar flagellum. Obligate aerobes. Optimum temperature 30–37 °C for mesophilic species and 50–53 °C for the moderately thermophilic species. Optimum pH between 3 and 6. The recognized species are facultative chemolithoautotrophs; optimum growth typically occurs in mixotrophic media supplemented with reduced sulfur compounds and organic supplements (yeast extract, peptone, some sugars or amino acids). Chemo-organotrophic growth is obtained on yeast extract, Casamino acids, peptone and meat extract. Most strains can grow chemolithoautotrophically with thiosulfate, tetrathionate, elemental sulfur or H2S. Some strains can grow on carbon disulfide, dimethylsulfide or dimethyldisulfide as energy sources. Some strains oxidize ferrous iron [Fe(II)] and arsenite [As(III)], and some can oxidize and grow on metal sulfides, including chalcopyrite, arsenopyrite, sphalerite, galena and some synthetic sulfides. Sensitive to ampicillin. Major ubiquinone is Q-8. DNA G+C content is 61–69 mol%. Members of the Betaproteobacteria. The type species is Thiomonas intermedia (London 1963) Moreira and Amils 1997 (=Thiobacillus intermedius London 1963).
Emended description of Thiomonas cuprina Moreira and Amils 1997
The emended description here is essentially that of ‘Thiobacillus cuprinus’ given by Huber & Stetter (1990), as emended by Moreira & Amils (1997), Kelly & Wood (2005) and in this study. Cells are Gram-negative, aerobic rods, 1.0–4.0 µm long and 0.3–0.5 µm wide; motile with a single polar flagellum. Brownish-coloured colonies develop on complex media (yeast extract, peptone, Casamino acids, meat extract). Temperature optimum is 30–36 °C; no growth at 15 or 50 °C. Optimum pH for growth on yeast extract or sulfidic ores is pH 3.0–4.0, with a typical range of pH 2.0–6.5; no growth at pH 1.0 or 7.4. Some strains can grow on yeast extract or sulfide ores at pH 1.5–4.5. Facultative chemolithoautotrophs; aerobic. Chemo-organotrophic growth on yeast extract, peptone, Casamino acids and meat extract; some strains grow on pyruvate. No currently reported strains can grow on arabinose, fructose, galactose, glucose, lactose, mannose, raffinose, ribose, sorbose, sucrose, arginine, cysteine, glycine, L-glutamate, L-lysine, DL-serine, acetate, lactate, succinate, citrate or malate. Chemolithoautotrophic growth on a defined mixture of sulfide ores, chalcopyrite or arsenopyrite, or H2S, and less efficiently on single sulfide ores (sphalerite, galena and synthetic CdS and FeS) or elemental sulfur. No growth on the natural ores bornite, chalcocite, covellite, pyrite, pitchblende or cinnabar or the synthetic sulfides Ag2S, CuS, MoS, Sb2S3, SnS or ZnS. Ferrous sulfate is neither oxidized nor used as a growth substrate. Copper, zinc and uranium can be mobilized from ore mixtures and high levels of resistance are exhibited to cobalt, nickel and zinc, with significant tolerance of copper, arsenic and uranium. Sensitive to ampicillin. Contains ubiquinone Q-8 and meso-diaminopimelic acid, but not rusticyanin. Found in continental solfataric fields and mining environments.
The type strain is strain Hö5T (=DSM 5495T =NBRC 102145T =NBRC 102094T). The G+C content of the DNA of the type strain is 66.0±0.6 mol% (Tm, HPLC). The 16S rRNA gene sequence of the type strain is deposited under GenBank/EMBL/DDBJ accession numbers AB331954 and AB331953.
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