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1 Department of Environmental and Natural Resource Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan
2 NITE Biological Resource Center, National Institute of Technology and Evaluation, 2-5-8 Kazusakamatari, Kisarazu-shi, Chiba 292-0818, Japan
3 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
4 Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
Correspondence
Donovan P. Kelly
D.P.Kelly{at}warwick.ac.uk
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-1 subgroup of the Betaproteobacteria (Moreira & Amils, 1997
). All four species (Thiomonas intermedia, Thiomonas perometabolis, Thiomonas thermosulfata and Thiomonas cuprina) were previously assigned to Thiobacillus but were found, by comparison of 5S and 16S rRNA gene sequences and by restriction fragment length analysis, to be rather remote from members of that genus (Moreira & Amils, 1997). Their closest phylogenetic neighbours within Thiobacillus were Thiobacillus thioparus and Thiobacillus denitrificans, which are in the -2 subgroup of the Betaproteobacteria (Lane et al., 1992). The 16S rRNA gene sequence similarity between Thiobacillus thioparus and Thiomonas intermedia was only 87 %. Additional defining characteristics of the four Thiomonas species included the G+C content of their DNA being between 61 and 69 mol%, the presence of ubiquinone Q-8, the inability to denitrify nitrate to dinitrogen and optimum growth as mixotrophs when supplied with both a reduced inorganic sulfur compound and a variety of organic substrates, but the ability also to grow chemolithoautotrophically or as chemo-organotrophs (Katayama-Fujimura et al., 1982, 1984; Moreira & Amils, 1997).
Moreira & Amils (1997) did not include Thiobacillus delicatus in the new genus as Thiomonas delicata, as insufficient phylogenetic data were then available, but they indicated that its affiliation with this mixotrophic group needed further investigation. Thiobacillus delicatus was originally isolated and characterized about 30 years ago (Mizoguchi et al., 1976; Katayama-Fujimura et al., 1982) and the name was formally revived with an emended species description by Katayama-Fujimura et al. (1984). It was retained in the list of species of the genus Thiobacillus in the 1989 and 2005 editions of Bergey's Manual of Systematic Bacteriology (Kelly & Harrison, 1989; Kelly et al., 2005). However, Kelly & Wood (2005) proposed that Thiobacillus delicatus should also be transferred to the genus Thiomonas as Thiomonas delicata, on the basis of its physiological and biochemical properties (Table 1), subject to its phylogenetic relationship being confirmed by 16S rRNA gene sequencing (Kelly et al., 2005; Kelly & Wood, 2005). This has now been done and we report that Thiobacillus delicatus should henceforth be known as Thiomonas delicata (Kelly & Wood, 2005, 2006).
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). Comparison with database sequences for other Thiomonas species using the BLAST algorithm (http://www.ncbi.nlm.nih.gov/blast/; Altschul et al., 1997) showed 99.9 % similarity of the Thiomonas delicata sequence with that of ‘Thiomonas arsenivorans’ (Battaglia-Brunet et al., 2006) and with those of Thiomonas sp. strain RCASK1 (AJ879998), Thiomonas sp. C19 (AF460989) and Thiomonas sp. CO2 (AF460988), with similarities of 93.4 % with Thiomonas intermedia and Thiomonas perometabolis, 91.1 % with Thiomonas thermosulfata and 88.8 % with Thiomonas cuprina (Fig. 1).
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). In particular, Thiomonas delicata has the following properties that are not shared with ‘Thiomonas arsenivorans’: it is non-motile, has more restricted ranges of temperature and pH for growth and optimum growth, can grow as an anaerobe using nitrate reduction to nitrite, but does not show heterotrophic growth on single organic compounds (glucose, fructose, ethanol, propanol, glycerol, oxalate, gluconate, pyruvate, lactate, malate, succinate, 2-oxoglutarate, citrate, alanine, serine, aspartate, glutamate, proline and histidine). Whereas ‘Thiomonas arsenivorans’ grows autotrophically on arsenite and chemo-organotrophically on a wide range of organic acids and sugars (Battaglia-Brunet et al., 2006), best growth of Thiomonas delicata is obtained on mixotrophic media with thiosulfate supplemented with Krebs cycle intermediates or amino acids. Optimal growth as a mixotroph is a property reportedly shared with Thiomonas intermedia, Thiomonas perometabolis, Thiomonas thermosulfata and Thiomonas cuprina (Moreira & Amils, 1997; Kelly & Wood, 2005). Whereas ‘Thiomonas arsenivorans’ can grow well on yeast extract, Thiomonas delicata gave virtually no growth with 0.1 % (w/v) yeast extract alone (about 5 mg cell protein l–1), but supplementing with 0.5 % (w/v) thiosulfate increased the biomass production to 90 mg cell protein l–1, compared with about 40 mg cell protein l–1 with thiosulfate alone (Mizoguchi et al., 1976). With 0.5 % (w/v) yeast extract, the biomass production was stimulated to about sixfold over that with thiosulfate alone (Katayama-Fujimura et al., 1984). While these properties suggest that Thiomonas delicata and ‘Thiomonas arsenivorans’ are separate species, determination of the ability of Thiomonas delicata to oxidize Fe(II) and As(III) and DNA–DNA hybridization between them will help to establish whether ‘Thiomonas arsenivorans’ is a distinct species or a subspecies of Thiomonas delicata. In this respect, it is noteworthy that the 16S rRNA gene sequences of Thiomonas intermedia and Thiomonas perometabolis also differ by only four nucleotides (99.7 % similarity), but were shown by DNA–DNA hybridization, 23S rRNA gene and restriction fragment length polymorphism to be distinct species (Katayama-Fujimura et al., 1982; Kelly & Harrison, 1989; Moreira & Amils, 1997).
The name Thiomonas delicata (Kelly & Wood, 2006) will have taxonomic precedence when validating the names of existing and future isolates of Thiomonas that are indistinguishable from it on the basis of their 16S rRNA gene sequences. Such isolates will require assessment of their physiological characteristics and comparative DNA–DNA hybridization with Thiomonas delicata. In this respect, there are numerous examples of species, in some cases from the same habitats, which share virtually identical 16S rRNA gene sequences (99–100 %) but show only 0–35 % interspecies DNA–DNA hybridization (Ash et al., 1991; Fox et al., 1992; Martinez-Murcia et al., 1992; Jaspers & Overmann, 2004).
Thiomonas species can also exhibit extremely divergent 16S rRNA gene sequences, as is seen with Thiomonas cuprina, which shows only 85.9–88.8 % sequence similarity with the other four Thiomonas species with validly published names. All five species have a rather distant relationship with strains of the -1 betaproteobacterium Burkholderia cepacia (87–90 % similarity) but, apart from Thiomonas cuprina, they show 91.1–99.7 % similarity with each other. On the basis of physiological properties and molecular analyses, Moreira & Amils (1997) argued that Thiomonas cuprina should be included in the genus Thiomonas. However, the current wealth of betaproteobacterial 16S RNA gene sequences indicates that Thiomonas cuprina is not securely placed as a recognized member of the Thiomonas clade on phylogenetic trees, being at least as closely related to B. cepacia and some other genera as to the Thiomonas cluster (Fig. 1; Y. Uchino, additional data not shown). None of the recognized species (or ‘Thiomonas arsenivorans’), except Thiomonas cuprina, has been reported to be capable of autotrophic growth on sulfide minerals. Moreira & Amils (1997) erroneously stated that Thiomonas cuprina also could not grow on sulfide minerals, but the type strain grew autotrophically on arsenopyrite, chalcopyrite, galena, cadmium sulfide and synthetic FeS (Huber & Stetter, 1990), although it did not oxidize Fe(II). In contrast to the other species of Thiomonas described to date, it could not grow on thiosulfate or tetrathionate as energy substrates, being able to use only more reduced sulfur substrates such as elemental sulfur and sulfides. With the exception of ‘Thiobacillus plumbophilus’ (Drobner et al., 1992), this inability to use thiosulfate is unique among all the species currently and previously known as Thiobacillus (Kelly & Harrison, 1989; Kelly et al., 2005) and other chemolithotrophic thiosulfate-oxidizing Proteobacteria such as Paracoccus, Pseudaminobacter and Thiomicrospira. However, Thiomonas cuprina and ‘Thiobacillus plumbophilus’ are not closely related phylogenetically, as they show insignificant DNA–DNA hybridization (Drobner et al., 1992) and share only about 85 % 16S rRNA gene sequence similarity (estimated by BLAST2 sequence comparison). Also, contrary to the description of Thiomonas cuprina provided by Moreira & Amils (1997), Huber & Stetter (1990) did not report that this species grew best under mixotrophic conditions. Unlike other Thiomonas species, the type strain of Thiomonas cuprina is moderately acidophilic with some strains being extreme acidophiles (Huber & Stetter, 1990). As well as sharing only 86–89 % 16S rRNA gene sequence similarity with the other Thiomonas species, Thiomonas cuprina shows only 85–89 % sequence similarity with other phylogenetically related Betaproteobacteria, including the type strains of B. cepacia, Leptothrix discophora and Comamonas testosteroni. Thiomonas cuprina also shares 87.5 % similarity of its 23S rRNA gene sequence with that of B. cepacia (Moreira & Amils, 1996). Currently, Thiomonas cuprina appears to have no closer phylogenetic neighbours than these genera (Moreira & Amils, 1997; D. P. Kelly, unpublished sequence analyses). It clearly differs from B. cepacia at the genus level (Selenska-Pobell et al., 1998). There is thus a case for considering the promotion of Thiomonas cuprina as representing a novel genus of moderately acidophilic, metal sulfide-oxidizing, facultatively chemolithoautotrophic Betaproteobacteria.
The description of Thiomonas delicata is essentially that provisionally proposed by Kelly & Wood (2005), based on that of Katayama-Fujimura et al. (1984), as emended below. The type strain is available from the NBRC (Japan), the Korean Collection of Type Cultures (KCTC) and the DSMZ.
Emended description of Thiomonas delicata (Katayama-Fujimura et al. 1984) Kelly and Wood 2006
Thiomonas delicata (del.i.cat'a. L. fem. adj. delicata delicate).
Basonym: Thiobacillus delicatus (ex Mizoguchi et al. 1976) Katayama-Fujimura et al. 1984.
Rods, usually single, rarely in pairs, 0.4–0.6 µm wide and 1.0–1.6 µm long. Non-motile. Colonies grown on yeast extract-thiosulfate agar (1 mm in diameter) are smooth and circular and change from transparent to whitish-yellow with sulfur. Facultative chemolithotroph and mixotroph. Grows autotrophically with sulfur, thiosulfate and tetrathionate, but not with thiocyanate; accumulates tetrathionate and trithionate transiently during growth on thiosulfate. Incapable of chemo-organotrophic growth on single carbon compounds. Grows mixotrophically with thiosulfate as an energy source in mineral media supplemented with tricarboxylic acid cycle intermediates, amino acids or yeast extract. Optimum growth requires both organic substances and thiosulfate or sulfur. Facultative anaerobe; reduces nitrate and produces nitrite in mixotrophic and autotrophic media with thiosulfate or tetrathionate, but does not denitrify nitrate to nitrogen gas. Ammonium salts, nitrate, urea, glutamate or aspartate can be used as a nitrogen source. Optimum temperature, 30–35 °C; growth range, 15–42 °C (no growth at 10 or 45 °C). Optimum pH, 5.5–6.0; growth range, pH 5.0–7.0. Isolated from mine water. Distribution unknown. The G+C content of the DNA is 66–67 mol% (Tm, chemical analysis).
The type strain is THI 091T [=NBRC 14566T (formerly IFO 14566T)=KCTC 2851T=DSM 17897T]. The culture deposited as IAM 12624T is no longer available from that collection.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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