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Desulfotomaculum carboxydivorans sp. nov., a novel sulfate-reducing bacterium capable of growth at 100 % CO

¹ Laboratory of Microbiology of Anthropogenic Environments, Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospect 60 let Oktyabrya 7 b. 2, Moscow, Russia
² Sub-Department of Environmental Technology, Wageningen University, Bomenweg 2, PO Box 8129, 6700 EV Wageningen, The Netherlands
³ Laboratory of Microbiology, Wageningen University, Hesselink van Suchtelenweg 4, 6703 CT Wageningen, The Netherlands

Correspondence
Sofiya N. Parshina
sonjaparshina{at}mail.ru

	ABSTRACT

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A moderately thermophilic, anaerobic, chemolithoheterotrophic, sulfate-reducing bacterium, strain CO-1-SRB^T, was isolated from sludge from an anaerobic bioreactor treating paper mill wastewater. Cells were Gram-positive, motile, spore-forming rods. The temperature range for growth was 30–68 °C, with an optimum at 55 °C. The NaCl concentration range for growth was 0–17 g l^–1; there was no change in growth rate until the NaCl concentration reached 8 g l^–1. The pH range for growth was 6·0–8·0, with an optimum of 6·8–7·2. The bacterium could grow with 100 % CO in the gas phase. With sulfate, CO was converted to H₂ and CO₂ and part of the H₂ was used for sulfate reduction; without sulfate, CO was completely converted to H₂ and CO₂. With sulfate, strain CO-1-SRB^T utilized H₂/CO₂, pyruvate, glucose, fructose, maltose, lactate, serine, alanine, ethanol and glycerol. The strain fermented pyruvate, lactate, glucose and fructose. Yeast extract was necessary for growth. Sulfate, thiosulfate and sulfite were used as electron acceptors, whereas elemental sulfur and nitrate were not. A phylogenetic analysis of 16S rRNA gene sequences placed strain CO-1-SRB^T in the genus Desulfotomaculum, closely resembling Desulfotomaculum nigrificans DSM 574^T and Desulfotomaculum sp. RHT-3 (99 and 100 % similarity, respectively). However, the latter strains were completely inhibited above 20 and 50 % CO in the gas phase, respectively, and were unable to ferment CO, lactate or glucose in the absence of sulfate. DNA–DNA hybridization of strain CO-1-SRB^T with D. nigrificans and Desulfotomaculum sp. RHT-3 showed 53 and 60 % relatedness, respectively. On the basis of phylogenetic and physiological features, it is suggested that strain CO-1-SRB^T represents a novel species within the genus Desulfotomaculum, for which the name Desulfotomaculum carboxydivorans is proposed. This is the first description of a sulfate-reducing micro-organism that is capable of growth under an atmosphere of pure CO with and without sulfate. The type strain is CO-1-SRB^T (=DSM 14880^T=VKM B-2319^T).

	MAIN TEXT

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Anaerobic conversion of CO has been reported for a large number of micro-organisms, including phototrophs, homoacetogens, methanogens and sulfate-reducers (Mörsdorf et al., 1992; Davidova et al., 1994). Several anaerobic hydrogenogenic thermophilic bacteria that were able to convert CO to H₂/CO₂ have been isolated from different natural habitats (Svetlichny et al., 1991, 1994; Sokolova et al., 2001, 2002, 2004a). Recently, the first hyperthermophilic archaeon capable of hydrogenogenic CO conversion was described (Sokolova et al., 2004b). Most of the recently described carboxydotrophic bacteria grow at a high partial pressure of CO, despite the fact that these conditions are never encountered in the environment.

In contrast to the so-called hydrogenogens (Svetlitchnyi et al., 2001), most anaerobic micro-organisms metabolizing CO are sensitive to high levels of CO. Sulfate-reducing bacteria in particular are considered to be very sensitive to CO (Mörsdorf et al., 1992; Davidova et al., 1994). Several sulfate-reducing bacteria are able to convert CO at concentrations of up to 20 %, but higher concentrations completely inhibit growth (Lupton et al., 1984; Klemps et al., 1985; Karpilova et al., 1983; Mörsdorf et al., 1992; Davidova et al., 1994). Our recent experiments with several strains of thermophilic sulfate-reducing bacteria have demonstrated that Desulfotomaculum kuznetsovii and Desulfotomaculum thermobenzoicum subsp. thermosyntrophicum are able to use CO as a sole carbon and energy source at concentrations of up to 50 % CO in the gas phase and are able to reduce sulfate with CO (Parshina et al., 2005). To date, no sulfate-reducing bacterium, growing on pure CO, has been isolated.

Batch experiments at a moderately elevated temperature (55 °C) with several mesophilic anaerobic sludges have revealed the presence of viable populations of fast-growing hydrogenogenic CO-oxidizing bacteria (Sipma et al., 2003). To date, anaerobic hydrogenogenic CO-converting micro-organisms have only been isolated from high-temperature volcanic environments that contain small amounts of CO (Symonds et al., 1994). The presence of hydrogenogenic, moderately thermophilic CO-converting bacteria in anaerobic bioreactors, where in situ CO concentrations are presumed to be negligible, is very interesting and has not been observed before. Furthermore, sulfate-reducing activity at high CO concentrations (up to 100 % CO and 180 kPa) has also not been reported previously.

We describe the isolation and characterization of a novel moderately thermophilic, sulfate-reducing bacterium that is able to grow at 100 % CO. Anaerobic granular (methanogenic) sludge samples were obtained from a full-scale anaerobic reactor treating wastewater from several paper mills (Industriewater Eerbeek BV., Eerbeek, The Netherlands). This sludge was originally cultivated at 30–35 °C. CO conversion by this sludge has been described previously (Sipma et al., 2004).

To obtain an enrichment of hydrogenogenic CO-converting bacteria, bottles containing crushed Eerbeek sludge were incubated at 55 °C. A suspension of crushed granules was obtained as reported previously (Sipma et al., 2003) and cultivated in a liquid medium. The medium was prepared as described by Parshina et al. (2005). After a few series of dilutions under an atmosphere of 100 % CO (at 120–180 kPa), an enriched culture was obtained that contained at least three morphologically different bacteria. The morphology of one of the strains resembled that of the spore-forming sulfate-reducing bacteria investigated by Parshina et al. (2005). The addition of 20 mM sodium sulfate to the dilution series under 100 % CO resulted in a suspension of morphologically identical cells. Roll-tubes containing the same medium supplemented with 5 % agar and pure CO in the gas phase were prepared in order to obtain separate colonies. Some of the colonies obtained were subsequently inoculated in the liquid medium. One of these cultures, CO-1-SRB^T, was selected for further study.

Desulfotomaculum nigrificans DSM 574^T was obtained from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany, and Desulfotomaculum sp. RHT-3 (Mori et al., 2000) was kindly provided by Professor K. Takamizawa (Gifu University, Japan). These strains were cultivated in medium supplemented with pyruvate or under an atmosphere of H₂/CO₂ in the presence of sulfate.

CO (purity 99·997 %) was supplied by Hoek Loos. Medium preparation and analytical methods used were as described by Parshina et al. (2003, 2005). CO₂ analysis was performed according to Henstra & Stams (2004). Desulfoviridin was analysed using the method of Postgate (1979). In common with D. nigrificans DSM 574^T, strain CO-1-SRB^T did not contain desulfoviridin.

Cells of strain CO-1-SRB^T were rod-shaped with rounded ends (0·5–1·5 µm thick and 5–15 µm long) and sometimes occurred in pairs. Cells were motile with a ‘twisting and tumbling’ motion. Strain CO-1-SRB^T formed oval spores that were terminal or subterminal. After 6 days of growth in agar medium with glucose, rhizoid black colonies with a diameter of 0·5 mm were obtained. The purity of the strain was checked by phase-contrast microscopy after cultivation on CO, H₂/CO₂ and glucose (with and without sulfate).

Unless otherwise stated, experiments were performed in duplicate. Growth was assessed by measuring the OD₆₆₀ and by monitoring substrate consumption and product formation. The temperature, pH and NaCl ranges were determined in stationary cultures with CO. To determine the pH range, medium was prepared with 50 mM phosphate buffer and adjusted by adding 6 M HCl or 6 M NaOH.

Strain CO-1-SRB^T grew between 30 and 68 °C, with an optimum temperature of 55 °C. Growth occurred between 0 and 17 g NaCl l^–1; at concentrations higher than 8 g NaCl l^–1, the growth rate was reduced. Growth occurred between pH 6·0 and 8·0, with an optimum between 6·8 and 7·2. The following possible electron donors for growth were tested (20 mM unless otherwise indicated): pyruvate, lactate, glucose, fructose, sucrose, maltose, galactose, serine, alanine, acetate, formate, butyrate, fumarate, benzoate, ethylene glycol, cellobiose, amorphous cellulose (2 g l^–1), methanol, ethanol, propanol, butanol, H₂/CO₂ (80 : 20 %) and CO (100 %) with (20 mM) and without sulfate. Potential electron acceptors that were tested included sulfate (20 mM), thiosulfate (20 mM), sulfite (2 mM), nitrate (10 mM) and sulfur (2 g l^–1). Growth in the presence of sulfate was found with CO (100 %), H₂/CO₂, pyruvate, glucose, fructose, maltose, lactate, alanine, serine, ethanol and glycerol. Very weak growth was observed on yeast extract alone (2 g l^–1) plus sulfate. Growth in the absence of sulfate was found with CO (100 %), pyruvate, lactate, glucose and fructose. No growth in the presence of sulfate was observed on acetate, malate, fumarate, benzoate, cellobiose, galactose, maltose, butyrate or ethylene glycol. In the absence of sulfate, no growth was observed on acetate, malate, fumarate, glycerol, alanine, ethanol, methanol, formate, butyrate, benzoate, cellobiose, galactose or ethylene glycol. Growth with sulfate, thiosulfate and sulfite as the electron acceptor was observed using lactate as the electron donor, whereas no growth was found with sulfur and nitrate. Glucose was degraded to hydrogen and acetate. Yeast extract (0·5 g l^–1) was necessary for growth.

Fig. 1 shows CO conversion by strain CO-1-SRB^T with 100 % CO, in the absence and presence of sulfate. The CO conversion rates were similar. Pure CO was converted with stoichiometric production of H₂ and CO₂ (CO₂ was not analysed during the course of this experiment and is therefore not shown). The OD₆₆₀ at the end of growth was 0·15. In the medium with sulfate, hydrogen and H₂S (up to 6 mM) were formed and a final OD₆₆₀ of 0·32 was obtained. No other products were formed during CO conversion.

View larger version (14K): [in this window] [in a new window]   Fig. 1. CO () conversion and H2 () and H2S () formation by strain CO-1-SRBT under an atmosphere of 100 % CO in the absence (a) and presence (b) of sulfate.

Gas chromatography-mass spectrometry (GC-MS) analysis was performed using a GC-MS system (AT-5973B; Agilent Technology) with a cross-linked methyl silicone capillary column (HP-5MS, Hewlett Packard). The oven temperature was programmed for 2 min at 120 °C, rising to 280 °C at 5 °C min^–1. Samples (1–2 µl) were injected into the GC at 280 °C. Fatty acids and other lipid components were ionized by electron impact at 70 eV after separation in the GC column and analysed in the scan mode. The quadruple mass spectrometer had a resolution of 0·5 mass units over the whole mass range of 2–550 atomic mass units. The sensitivity of the GC-MS system was 0·01 ng methyl stearate. Each substance was confirmed by its mass spectrum and by a search of the NIST mass spectral database library.

A comparison of the fatty acid profiles of strains CO-1-SRB^T, D. nigrificans DSM 574^T and Desulfotomaculum sp. RHT-3 is presented in Table 1. All three strains were cultivated in the same medium with pyruvate plus sulfate. Strain CO-1-SRB^T contained saturated and unsaturated fatty acids as well as hydroxylated fatty acids. All strains contained fatty acids common for Desulfotomaculum species (Ueki & Suto, 1979; Hagenauer et al., 1997; Liu et al., 1997; Love et al., 1993). The strains showed some quantitative differences in the fatty acid content. Fatty acids iso 14 : 0, iso 15 : 1, anteiso 16 : 1 and iso 16 : 0 aldehyde were absent in D. nigrificans and present only in trace amounts in strain RHT-3 (Table 1). Fatty acids from iso 18 : 0 aldehyde up to anteiso 19 : 0 were absent in D. nigrificans DSM 574^T but present in strain RHT-3. Fatty acids 17 : 1 aldehyde and 17 : 0 aldehyde were found only in strain RHT-3.

Analysis of the 16S rRNA gene sequence of the isolate was performed by the DSMZ Identification Service, as described previously (Parshina et al., 2003).

Sequence similarity searches were performed using the BLAST algorithm (http://www.ncbi.nih.gov/blast/; Altschul et al., 1990). Phylogenetic analysis and tree construction (Fig. 2) were performed with programs from the ARB software package (Ludwig et al., 2004). The phylogenetic tree was constructed using the neighbour-joining method (Saitou & Nei, 1987) and was based on the results of distance matrix analysis including only those nucleotides between Escherichia coli positions 49 to 1387 that are conserved in at least 50 % of sequences from relevant members of Gram-positive bacteria. The topology of the tree was confirmed using maximum-parsimony and maximum-likelihood methods as implemented in the ARB program package.

View larger version (31K): [in this window] [in a new window]   Fig. 2. 16S rRNA gene sequence-based phylogenetic tree constructed by the neighbour-joining method (Saitou & Nei, 1987) as implemented in the ARB software package (Ludwig et al., 2004) using E. coli positions 49 to 1387 and showing the position of strain CO-1-SRBT in relation to members of the genus Desulfotomaculum. GenBank accession numbers are given in parentheses. Bar, 10 % divergence.

Phylogenetic analysis revealed that strain CO-1-SRB^T is highly related to D. nigrificans (99 %), based on their 16S rRNA gene sequences. Comparisons of the 16S rRNA gene sequences of CO-1-SRB^T with close relatives revealed the following similarities: D. acetoxidans (88·2%), D. ruminis (93·1 %), D. putei (93·7 %), D. aeronauticum (93·9 %), D. nigrificans (99 %) and Desulfotomaculum sp. RHT-3 (100 %). DNA–DNA hybridization of strain CO-1-SRB^T with D. nigrificans DSM 574^T showed 70·5 % relatedness (DSMZ analysis) and 53 % (INMI). The DNA–DNA relatedness of CO-1-SRB^T to strain RHT-3 was 60 % (INMI analysis). For D. nigrificans DSM 574^T, DNA–DNA relatedness to strain RHT-3 was 61 % (DSMZ) and 52 % (INMI). The DNA G+C content of D. nigrificans DSM 574^T was higher than that of strain CO-1-SRB^T and strain RHT-3. The DNA–DNA hybridization values of all three strains were lower than 70 %, the value suggested for species discrimination (Wayne et al., 1987).

A morphological and physiological comparison of the phylogenetically related strains is presented in Table 2. D. acetoxidans, D. ruminis and D. aeronauticum are mesophilic, with a temperature optimum of 36–37 °C (Table 2). D. putei is thermophilic, but does not grow on glucose or fructose plus sulfate and does not ferment lactate, glucose or fructose. D. nigrificans does not grow on glycerol plus sulfate and does not ferment lactate. Desulfotomaculum sp. RHT-3 does not utilize ethanol in the presence of sulfate. Unfortunately, only a few substrates have been tested for strain RHT-3 (Mori et al., 2000); therefore, we tested the strain in CO in the presence and absence of sulfate. Isolate CO-1-SRB^T was able to grow on ethanol plus sulfate and grew weakly on glycerol plus sulfate. Furthermore, strain CO-1-SRB^T could actively ferment lactate, glucose and fructose. The most remarkable difference was the ability to oxidize CO. In a direct comparison with strain CO-1-SRB^T, both D. nigrificans DSM 574^T and strain RHT-3 were unable to oxidize CO without sulfate. In the presence of sulfate, D. nigrificans DSM 574^T could grow at a CO concentration of 5–20 %, but not higher, confirming the data of Klemps et al. (1985). Moreover, we found that Desulfotomaculum sp. RHT-3 was not able to grow at a CO concentration exceeding 50 %. Strain CO-1-SRB^T could grow on CO both in the presence and in the absence of sulfate. During the growth of D. nigrificans DSM 574^T and Desulfotomaculum sp. RHT-3 in CO, hydrogen was never detected in the gas phase. This suggests that these strains use CO directly for sulfate reduction without the intermediate formation of hydrogen, as has been also reported recently for D. kuznetsovii and D. thermobenzoicum subsp. thermosyntrophicum (Parshina et al., 2005). During the growth of strain CO-1-SRB^T at all studied CO concentrations (5–100 %) with sulfate, hydrogen was always an intermediate. During growth in CO without sulfate, hydrogen and CO₂ were the only products of CO conversion.

Description of Desulfotomaculum carboxydivorans sp. nov.
Desulfotomaculum carboxydivorans (car.bo.xy.di.vor'ans. N.L. n. carboxydum carbon monoxide; L. part. adj. vorans devouring; N.L. part. adj. carboxydivorans carbon monoxide digesting).

Cells are rod-shaped with rounded ends, 0·5–1·5x5–15 µm, single or sometimes paired. Cells are motile with ‘twisting and tumbling’ movements. Cells form oval spores, terminal or subterminal. CO (100 % in the gas phase) can serve as a sole electron donor both in the presence and absence of sulfate. Other substrates utilized with sulfate are H₂/CO₂, pyruvate, lactate, glucose, fructose, maltose, ethanol, glycerol, alanine and serine. The bacterium ferments pyruvate, lactate, glucose and fructose. The optimum pH is 6·8–7·2; the optimum temperature is 55 °C. The optimum NaCl concentration is 0–8 g l^–1. The DNA G+C content is 45·6 mol%.

The type strain, CO-1-SRB^T (=DSM 14880^T=VKM B-2319^T), was isolated from sludge from an anaerobic bioreactor treating paper mill wastewater.

	ACKNOWLEDGEMENTS

 
We are grateful to Professor K. Takamizawa for the gift of Desulfotomaculum strain RHT-3, Dr George Osipov for cellular fatty acid analyses and Dr Cathrin Spröer and Dr Peter Schumann (DSMZ) for DNA analysis. This research was financially supported by a grant (STW-WBC 5280) from the Technology Foundation (STW) of the Netherlands Organization of Scientific Research (NWO), The Netherlands, by Paques Natural Solutions BV, Balk, The Netherlands, and by a Molecular Cell Biology grant from the Russian Academy of Sciences.

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