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Max-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany
Correspondence
Verona Vandieken
vvandiek{at}mpi-bremen.de
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ABSTRACT |
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, who isolated the marine species Desulfuromonas acetoxidans, which reduces elemental sulfur with acetate. The genus contains four further species, which had been isolated with reduction of iron, sulfur or tetrachloroethene from marine and freshwater sediments: Desulfuromonas palmitatis (Coates et al., 1995), Desulfuromonas acetexigens (Finster et al., 1994), Desulfuromonas thiophila (Finster et al., 1997) and Desulfuromonas chloroethenica (Krumholz, 1997; Krumholz et al., 1996). The genus Desulfuromusa is represented by three species, Desulfuromusa bakii, Desulfuromusa kysingii and Desulfuromusa succinoxidans, isolated by elemental sulfur reduction (Liesack & Finster, 1994). Together with the genera Pelobacter, Malonomonas and Geobacter, Desulfuromusa and Desulfuromonas form the family Geobacteraceae Holmes et al. 2004, a monophyletic group within the Deltaproteobacteria (Holmes et al., 2004a; Lonergan et al., 1996). An important characteristic of species within this group is the ability to reduce Fe(III) and/or elemental sulfur. Additionally, some species grow by fermentation or syntrophically (Cord-Ruwisch et al., 1998; Schink, 1984; Schink & Pfennig, 1982; Schink & Stieb, 1983). Due to the variety of metabolic pathways performed by isolated species of the Geobacteraceae, the in situ activity of this group remains unclear, since several constituents in freshwater and marine sediments can usually be utilized by these bacteria.
Strains were obtained from enrichment cultures inoculated with surface sediments of two fjords along the west coast of Svalbard with bottom water temperatures of 2–3 °C. Strains 49, 60, 102T and 103 originated from Tempelfjorden, Station CD (78° 25.267' N 17° 08.277' E; water depth 64 m) and strain 112T from Smeerenburgfjorden, Station J (79° 42.006' N 11° 05.199' E; water depth 212 m). Enrichment and isolation were performed in artificial sea-water medium (Widdel & Bak, 1992) with a reduced MgSO4.7H2O concentration of 0.4 mM to avoid growth of sulfate-reducing bacteria. Acetate (20 mM) and synthetically produced poorly crystalline iron oxide (
30 mM) (Lovley, 2000) were added for enrichments at 10 °C. For the isolation in deep-agar dilution technique (Isaksen & Teske, 1996), iron oxide was replaced with soluble ferric citrate (30 mM). For the determination of alternative substrates and salt, pH and vitamin requirements, growth medium with a lower salt concentration was used (salt-water medium) (Widdel & Bak, 1992). All physiological tests were performed in duplicate at 10 °C. Cultures growing with alternative substrates were transferred into fresh test medium for verification. Temperature tolerance of the strains was determined in an aluminium temperature-gradient block at 13 different temperatures between –2 and 30 °C (Sagemann et al., 1998). Salt requirements were determined in media with 12 different NaCl concentrations between 0.05 and 5 % (w/v) and 10 different MgCl2.6H2O concentrations between 0.02 and 3.6 % (w/v). The pH optima of the strains were determined in media with 12 different pH values (in triplicate) that covered a range from pH 5.5 to 8.3. For all tests, growth was monitored spectrophotometrically (Shimadzu UV 1202) by measuring the OD at 580 nm for cells grown on fumarate/acetate and by measuring Fe2+ accumulation (Stookey, 1970) for cells grown on ferric citrate/acetate. Reduction of ferric citrate was also tested in media with FeCl2.4H2O (2–3 mM end concentration) or cysteine (1 mM end concentration) as reducing agents instead of sulfide.
Malonomonas rubra DSM 5091T, obtained from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ, Braunschweig, Germany), was grown in salt-water medium with malonate as substrate. To test the ability of cells to grow by S0, Fe(III) or Mn(IV) reduction, malonate was replaced with ferric citrate, poorly crystalline iron oxide, manganese oxide or S0 as electron acceptor and acetate as electron donor.
Fatty acids were analysed by GC and GC-MS (Elvert et al., 2003). Lipoquinones, the G+C content of genomic DNA and DNA–DNA hybridization were determined at the DSMZ.
PCR amplification of 16S rRNA genes was performed with the primers 8F and 1492R and PCR products were amplified for sequence analysis with primers 8F, 341F, 518F, 534R, 1099F and 1492R (Buchholz-Cleven et al., 1997). The ARB program (Ludwig et al., 2004) was used for phylogenetic analysis.
Purity of cultures of strains 49, 60, 103, 112T and 102T was checked microscopically and by inoculating the cultures into media with yeast extract, casein, glucose or fructose. Strains 49, 60, 103 and 112T were all phylogenetically closely related (99.4–99.7 % 16S rRNA gene sequence similarity). The strains were tested for growth with a selection of environmentally important electron acceptors and donors and showed similar substrate spectra (data not shown). Furthermore, the strains all revealed similar optimum growth temperatures around 15 °C and growth at 0 °C (data not shown). Due to the similarities of strains 49, 60, 103 and 112T, strain 112T was selected for further detailed characterization. Strain 102T was also characterized in detail.
Cells of strains 112T and 102T grew as thin rods (Fig. 1). Cells of strain 112T were 0.7x2–3.5 µm and those of strain 102T were 0.7–1x3–5 µm in size. Cells of the latter strain formed clumps in liquid culture. Both strains stained Gram-negative and were non-spore-forming and motile. Electron microscopy (Zeiss EM 10 A; conducted at the UFT, University of Bremen) revealed peritrichous flagellation for strain 112T and monopolar lophotrichous flagellation for strain 102T (Fig. 1c).
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Strain 112T grew in the presence of ferric citrate with acetate, propionate, pyruvate, ethanol, propanol, butanol, proline and choline chloride as electron donors and strain 102T with acetate, lactate, formate, H2 (H2/CO2; 80 : 20, v/v), succinate, pyruvate, fumarate, ethanol, propanol, butanol and proline. Electron donors not used by either strain were butyrate, hexanoate, malate, succinate, citrate, fructose, glucose, glycerol, glycine, glutarate, alanine, serine, proline, betaine, sorbitol, nicotinate, yeast extract and casein; substrates not used by strain 112T were lactate, formate, fumarate, succinate and H2, and strain 102T did not use propionate or choline chloride. Both strains grew by reduction of Fe(III) compounds (ferric citrate and iron oxide tested) and fumarate in the presence of acetate. Additionally, the strains slowly reduced elemental sulfur and manganese oxide. Neither strain reduced sulfate, thiosulfate, sulfite, nitrate, nitrite, oxygen or malate. Ferric citrate was also reduced in media with FeCl2 or cysteine as reducing agents instead of sulfide. No reduction of Fe(III) in the presence of oxygen was observed for either strain. Disproportionation of sulfur or thiosulfate was not observed. Both strains grew with fumarate as the sole substrate, but not with lactate, malate, malonate, pyruvate, glucose or fructose. The major end product of fumarate disproportionation was succinate. Strain 102T did not require vitamins for growth, whereas strain 112T required biotin.
The phospholipid-derived ester-linked fatty acid composition of strains 112T and 102T is listed in Table 1. C16 : 1
7c and C16 : 0 were dominant as fatty acids in both strains, similar to the fatty acid composition of Geobacter metallireducens (Lovley et al., 1993). Cells of strain 112T contained MK-8 as the major menaquinone and traces of MK-9 (2 %); cells of strain 102T contained only MK-8. The DNA G+C contents were 50.1 mol% for strain 112T and 52.3 mol% for strain 102T.
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). Strain 112T was related to Desulfuromonas acetoxidans (97.0 % 16S rRNA gene sequence similarity), Desulfuromonas thiophila NZ27T (95.5 %), Pelobacter venetianus (93.7 %) and Desulfuromonas chloroethenica TT4BT (93.1 %). Species of the genus Desulfuromonas were isolated by reduction of elemental sulfur [Desulfuromonas acetoxidans (Pfennig & Biebl, 1976), Desulfuromonas acetexigens (Finster et al., 1994) and Desulfuromonas thiophila (Finster et al., 1997)], tetrachloroethene [Desulfuromonas chloroethenica (Krumholz, 1997; Krumholz et al., 1996) and ‘Desulfuromonas michiganensis’ (Sung et al., 2003)] or Fe(III) compounds [Desulfuromonas palmitatis (Coates et al., 1995)]. However, all species of this genus were able to reduce iron compounds and sulfur (Table 2). Strain 112T was most closely related to the marine species Desulfuromonas acetoxidans, which, similarly to strain 112T, was able to reduce elemental sulfur, Fe(III) and Mn(IV) (Pfennig & Biebl, 1976; Roden & Lovley, 1993). The two strains differed mainly in their temperature tolerance, with Desulfuromonas acetoxidans being mesophilic, growing between 25 and 35 °C, and strain 112T being psychrophilic, growing between –2 and 20 °C. Physiological differences between the two strains were the ability of strain 112T to oxidize propionate and to grow by disproportionation of fumarate and its inability to reduce malate (Table 2). DNA–DNA hybridization determined 22.7 % relatedness between strain 112T and Desulfuromonas acetoxidans DSM 684T. Therefore, we propose the description of strain 112T as the type strain of a novel species, Desulfuromonas svalbardensis sp. nov.
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), but cells did not grow by anaerobic respiration (Kolb et al., 1998). The ability of Malonomonas rubra to reduce iron compounds was described recently (Holmes et al., 2004a), and these authors suggested that Malonomonas rubra should be renamed as a member of the genus Desulfuromusa. This is supported by our results, as Malonomonas rubra DSM 5091T reduced ferric citrate, iron oxide, elemental sulfur and manganese oxide with acetate as electron donor (Table 3). Therefore, we propose strain 102T as the type strain of a novel species of the genus Desulfuromusa, Desulfuromusa ferrireducens sp. nov. The newly isolated strain 102T was psychrophilic, growing between –2 and 23 °C, whereas the other Desulfuromusa species do not grow below 4 °C and their optimum temperatures for growth are 
25 °C (Finster & Bak, 1993; Liesack & Finster, 1994). The psychrotolerant species Geopsychrobacter electrodiphilus is closely related to species of Desulfuromusa and Malonomonas rubra, but represents a unique phylogenetic cluster (Holmes et al., 2004b). Species of Desulfuromusa, Malonomonas rubra, strain 102T and Geopsychrobacter electrodiphilus share the ability to reduce elemental sulfur and Mn(IV) and oxidize acetate, succinate and pyruvate, but differ in the usage of other substrates (Table 3).
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; Bowman & McCuaig, 2003; Purdy et al., 2003; Mußmann et al., 2005). The isolation of strains 102T and 112T from marine sediments from Svalbard suggests that this group of bacteria is present in diverse freshwater and marine environments. Yet, the significance and in situ activity of the sulfur-/ferric iron-reducing members of the Geobacteraceae remains unclear for most habitats. As reviewed by Thamdrup (2000), ferric iron reduction is the second most important anaerobic respiration pathway in a wide range of habitats. In Arctic marine sediments of Svalbard, ferric iron reduction accounted for 0–26 % of the total carbon respiration (Kostka et al., 1999). Marine surface sediments that have a zone of reactive iron and manganese as well as accumulation of elemental sulfur provide optimal conditions for bacteria able to reduce these compounds, such as the strains described here. Such a sediment setting was, for example, described on the Danish coast, where the concentration of sulfur was highest in the zone of iron/manganese reduction (Sørensen & Jørgensen, 1987), due to the rapid reaction of H2S with Mn(IV) or Fe(III) to form elemental sulfur.
Possible substrates for Fe(III)-reducing bacteria are common fermentation products such as volatile short-chain fatty acids and hydrogen. Strains 112T and 102T oxidized important fermentation products such as acetate, lactate, formate or hydrogen concomitant with the reduction of Fe(III). Acetate is an important substrate for sulfate-reducing bacteria in temperate as well as Arctic marine sediments (e.g. Sørensen et al., 1981; Finke, 2003). Turnover rates in Arctic fjord sediments were highest for acetate, followed by lactate and propionate (Finke, 2003).
Psychrophilic sulfate-reducing bacteria isolated from Svalbard sediments showed constant growth yields between –2 °C and their optimum growth temperature (Knoblauch & Jørgensen, 1999). Among the Fe(III)-reducing bacteria, psychrophiles of the genus Shewanella have been isolated from the Antarctic, the Alboran Sea and deep-sea sediments of the Pacific Ocean, including Shewanella frigidimarina, Shewanella gelidimarina, Shewanella woodyi and Shewanella violacea (Bowman et al., 1997; Makemson et al., 1997; Nogi et al., 1998). The strains isolated by Fe(III) reduction in the present study grew at in situ temperatures just above the freezing point of sea water and were accordingly well adapted to the permanently low temperatures of the Arctic Ocean. Recently, the first psychrophilic and psychrotolerant species within the family Geobacteraceae have been isolated, Geopsychrobacter electrodiphilus and Geobacter psychrophilus (Holmes et al., 2004b; Nevin et al., 2005). Our isolates extend the group of psychrophiles within the Geobacteraceae.
In summary, the isolated strains were well suited to life in anoxic, permanently cold sediments of Svalbard. The abundance and diversity of Fe(III)- and sulfur-reducing bacteria in this environment have, however, not been investigated. More studies on the microbial communities and their in situ activities are needed to understand fully the importance of sulfur and Fe(III) reduction in marine sediments.
Description of Desulfuromonas svalbardensis sp. nov.
Desulfuromonas svalbardensis (sval.bard.en'sis. N.L. fem. adj. svalbardensis from Svalbard, a group of islands in the northern Barents Sea, from where the type strain was isolated).
Cells are rod-shaped, 0.7x2.5–3 µm, motile by peritrichous flagella. Gram-negative, strictly anaerobic and chemo-organotrophic. Biotin is required for growth. Grows by oxidation of acetate, propionate, ethanol, propanol, butanol, choline chloride or pyruvate with concomitant reduction of Fe(III). Fe(III) compounds, manganese oxide, elemental sulfur and fumarate serve as electron acceptors. Disproportionation of fumarate is observed. The pH range for growth is pH 6.5–7.5; optimum pH is 7.3. Psychrophilic, with an optimum growth temperature of 14 °C and a temperature range for growth of –2 to 20 °C. The DNA G+C content of the type strain is 50.1 mol%.
The type strain, strain 112T (=DSM 16958T=JCM 12927T), was isolated from a permanently cold fjord sediment of the west coast of Svalbard.
Description of Desulfuromusa ferrireducens sp. nov.
Desulfuromusa ferrireducens [fer.ri.re.du'cens. L. n. ferrum iron; L. part. adj. reducens leading back, bringing back and, in chemistry, converting to a reduced oxidation state; N.L. part. adj. ferrireducens reducing Fe(III) to Fe(II)].
Cells are rod-shaped, 0.7–1x3–5 µm, motile by monopolar lophotrichous flagella. Gram-negative, strictly anaerobic and chemo-organotrophic. No vitamins are required for growth. Oxidizes acetate, lactate, succinate, fumarate, pyruvate, proline, ethanol, propanol, butanol, formate or H2 with the reduction of Fe(III). Fe(III) compounds, elemental sulfur, manganese oxide and fumarate serve as electron acceptors. Disproportionation of fumarate is observed. The pH range for growth is pH 6.5–7.9; optimum is pH 7.0–7.3. Psychrophilic, with an optimum growth temperature of 14–17 °C and a temperature range for growth of –2 to 23 °C. The DNA G+C content of the type strain is 52.3 mol%.
The type strain, strain 102T (=DSM 16956T=JCM 12926T), was isolated from a permanently cold fjord sediment of the west coast of Svalbard.
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ACKNOWLEDGEMENTS |
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