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Department of Botany and Microbiology, Institute for Energy and the Environment, The University of Oklahoma, 770 Van Vleet Oval, Norman, OK 73019, USA
Correspondence
Joseph M. Suflita
jsuflita{at}ou.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains ALDCT and Lake are DQ303457 and DQ303458, respectively.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), whereas the other involves addition of the alkane to the double bond of fumarate with the formation of alkylsuccinic acid derivatives (Kropp et al., 2000; Rabus et al., 2001).
Several sulfate-reducing and denitrifying bacterial strains capable of the complete conversion of n-alkanes to CO2 have been isolated (Aeckersberg et al., 1991, 1998; Rueter et al., 1994; So & Young, 1999; Ehrenreich et al., 2000; Cravo-Laureau et al., 2004). A few of the novel strains have been fully characterized. All known alkane-degrading, nitrate-reducing bacteria (strains HxN1, OcN1 and HdN1) belong to the Betaproteobacteria Azoarcus/Thauera group and Deltaproteobacteria (Ehrenreich et al., 2000). All of the sulfate-reducing, alkane-degrading isolates are short oval-shaped rods belonging to the Deltaproteobacteria. Morphologically and physiologically, the sulfate-reducing isolates (with the exception of a thermophilic strain, TD3) are generally similar. However, phylogenetic comparison reveals substantive differences amongst the organisms. Comparison of 16S rRNA gene sequences reveals that several sulfate-reducing isolates cluster close to strain AK-01, including the mesophilic strains Pnd3, Hxd3 and the recently isolated Desulfatibacillum aliphaticivorans strain CV2803T. It has been suggested that these strains represent members of the genus Desulfatibacillum (Cravo-Laureau et al., 2004).
In this paper, we describe two novel alkane-degrading, sulfate-reducing bacteria, strain ALDCT, isolated from sludge collected from a naval oily wastewater-storage facility and strain Lake, isolated from production water from an oilfield in Oklahoma (USA). The two strains are phylogenetically close to each other but not to members of the genus Desulfatibacillum. We propose that strain ALDCT represents the type strain of a novel species and genus.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Enrichment and isolation.
Enrichment cultures yielding strain ALDCT were obtained using a basal sulfate-containing, brackish water mineral medium (Widdel & Bak, 1992), as described previously (Kropp et al., 2000). Anoxic incubation of produced water collected from an oil–water separation tank in the Bebee-Konawa oilfield actively reduced sulfate in the presence of crude oil. Cells from this water served as an inoculum for enrichments that ultimately yielded strain Lake. The Lake enrichments were obtained using the same basal sulfate-containing mineral medium, but for freshwater conditions (Widdel & Bak, 1992). After sterilization, the two media were supplemented with (per litre): 3.0 g NaHCO3 (from 10 % stock solution), 10 ml RST vitamin solution without mercaptoethansulfonic acid (Tanner, 1997), 0.05 g Na2S.9H2O and 0.05 g cysteine-HCl. The final pH was 7.2. Aliquots (25 ml) of the media were distributed in 160 ml serum bottles using anaerobic technique (Balch et al., 1979; Hungate, 1969) and were supplemented with 0.5 ml of an alkane mixture, comprising hexane/decane/dodecane/hexadecane (1 : 1 : 1 : 1, by vol.), which was supplied neat from anoxic (flushed with N2) and autoclaved stock solutions. The incubation bottles were sealed with Teflon-lined stoppers, secured with aluminium crimp seals and incubated inverted under a N2/CO2 (80 : 20) gas phase at 31 °C. Growth of the cultures was inferred by following the reduction of sulfate. Significant losses of electron acceptor (sulfate) relative to the substrate-unamended and sterile controls indicated the development of the desired activity. Positive incubations were used for further enrichment. After repeated transfers, stable cultures that contained cells of the same predominant morphology were obtained. These cultures were assayed for alkane loss as described previously (Kropp et al., 2000) and the stoichiometry of alkane consumption and sulfate reduction was determined. Cultures with the expected stoichiometry were selected for further purification.
Pure cultures were obtained by repeated serial dilution in basal seawater medium (Widdel & Bak, 1992), supplemented with RST trace metal solution (10 ml l–1) and modified RST vitamin solution (10 ml l–1) (Tanner, 1997) supplemented with 5.0 mg 6,8-thioctic acid l–1 instead of mercaptoethansulfonic acid. The final pH of the medium was 7.2–7.3. The medium was reduced with sodium sulfide and cysteine hydrochloride at initial concentrations of 100 mg l–1. Strains ALDCT and Lake were isolated using decane and hexane as growth substrates, respectively. Decane (5–10 mM) and hexane (7–10 mM) were provided in excess. The vials were incubated inverted at 31 °C and growth was assessed by both microscopy and sulfate depletion. The highest dilution at which growth occurred was used for the next dilution series. After repeated serial dilutions, pure cultures that contained cells of a single morphotype were obtained.
Purity controls.
Purity was checked by using phase-contrast microscopy and by inoculating the cultures in their usual cultivation medium containing glucose (10 mM), lactate (10 mM) and yeast extract (0.1 %) instead of an n-alkane. The lack of growth in these incubations suggested that no contaminants were present. In addition, the purity of the cultures was assessed by denaturing gradient gel electrophoresis (DGGE) (Muyzer et al., 1993; Duncan et al., 2003). Cultures that exhibited a single morphology and a single DGGE band were assumed to be pure and were selected for characterization. Pure cultures were maintained and characterized using the same medium as that used for isolation, with the respective alkanes as growth substrates.
Physiological characterization.
Incubation conditions promoting optimal growth rates were monitored as a function of sulfate consumption. Occasionally, growth was also followed as an increase in OD600. Sulfate was analysed by ion chromatography as described by Caldwell et al. (1998). Optimal salinity was determined using the basal medium with NaCl concentrations varying from 0 to 80 g l–1. The pH limits in the basal medium were adjusted with bicarbonate buffer (
). Growth at pH 4.5 and 5.5 was assayed in media containing the physiological buffers 20 mM homopipes [homopiperazine-N,N'-bis-2(ethanesulfonic acid); 20 mM, pKa=4.61] and 20 mM MES (20 mM; pKa=6.15), respectively.
Utilization of electron donors other than n-alkanes, as well as culture vitamin requirements, were tested under optimal conditions after at least three consecutive transfers. Water-soluble substrates were added from anoxic sterile stock solutions to provide the concentrations indicated below. Vitamins were filter-sterilized. Aromatic substrates and 4-methyloctanoic acid at the indicated concentrations were added neat. The polyaromatic substrates naphthalene and 2-methylnaphthalene were supplied as an overlay dissolved in 2,2,4,4,6,8,8-heptamethyl-nonane as a 10 mg ml–1 carrier. The ability to reduce electron acceptors was tested in basal seawater medium with decane as an electron donor, but without sulfate. For iron reduction experiments, the same medium was used except that the reducing agent was omitted. Iron reduction was determined with ferrozine reagent as described by Lovley & Phillips (1986) with both ferric citrate and ferric hydroxide as a source of Fe(III). Thiosulfate and sulfite were used at concentrations of 10 and 5 mM, respectively. Elemental sulfur (0.97 g l–1) was provided as polysulfide (Widdel & Pfennig, 1992). Reduction of elemental sulfur, sulfite and thiosulfate was determined by monitoring sulfide production. Sulfide was analysed according to Trüper & Schlegel (1964). All experiments were replicated and repeated.
The G+C content of the DNA was determined by using standard HPLC analysis (Mesbah et al., 1989) at the Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH (DSMZ). Genomic DNA was isolated using an Easy-DNA kit (Invitrogen).
PCR amplification of the 16S rRNA gene and phylogenetic analyses.
Nearly full-length 16S rRNA genes (Escherichia coli positions 8–1492) were obtained from DNA purified from cells by amplification with ‘universal’ eubacterial primers targeting conserved regions and the cycling conditions described by Herrick et al. (1993). Amplified DNA was purified from primers and unincorporated nucleotides and concentrated using Millipore Ultrafree-MC 30,000 NMWL Filter Devices to a concentration of 20–100 ng µl–1. Sequencing of the purified PCR products was performed at the University of Oklahoma DNA Sequencing Facility on an ABI model 377 automated sequencer, using Ampli-TaqFS DNA polymerase and fluorescence-labelled dNTPs in a cycle-sequencing kit (ABI Prizm Dye Terminator kit; PE Applied Biosystems). Amplification primers and two internal primers (704f, 907r; Johnson, 1994) were employed for sequencing of nearly full-length 16S rRNA genes. SEQUENCHER (Gene Codes) was used to assemble the fragments. The assembled sequence was compared with those in GenBank using BLASTN (Altschul et al., 1997; National Center for Biotechnology Information). Sequences from the BLASTN search that most closely matched the sequences of the clones and selected outgroup strains were aligned using CLUSTAL_X (v. 1.81) (Thompson et al., 1997). A dendrogram was constructed from the distance matrix using the neighbour-joining method in CLUSTAL_X and 1000 bootstrap replicates were performed to estimate the support for each branch (Felsenstein, 1985). Maximum-parsimony (1000 bootstrap replicates) and maximum-likelihood (100 bootstrap replicates) were used to confirm the phylogenetic placement of the cloned sequences (PAUP v. 4.0b10; Swofford, 2002).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Thus, 20.3 mM sulfate was consumed for 3 mM decane metabolized. This is 87 % of that theoretically expected according to the equation: |
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No acetate production was found with strain ALDCT or Lake during or after growth on hydrocarbons. The strains activated both protonated and deuterated n-alkanes by addition of the parent hydrocarbon to the double bond of fumarate (not shown) as described previously (Kropp et al., 2000; Davidova et al., 2005). Cells of strains ALDCT and Lake had similar morphologies and phylogenetic analysis showed that the organisms were closely related (see below). We focused on strain ALDCT for more detailed characterization.
Morphology
Cells of strain ALDCT stained Gram-negative and were slightly curved, short rods with oval ends (2.5–3.0x1.0–1.4 µm), often occurring in pairs. They tended to form aggregates or large clusters (Fig. 1a, b). Rod-shaped cells were more common at the exponential growth phase, whereas late cultures exhibited bigger and more round cells. The cells were non-motile and did not form endospores. Bacterial growth was often observed as a thin layer floating in the upper part of the aqueous phase adhering to the overlying hydrocarbon layer. Cell buoyancy may have been regulated by the gas vesicles that were observed under phase-contrast microscopy as refractile bodies in the middle of the cells. Gas vesicles have been reported for other hydrocarbon-degrading, sulfate-reducing bacteria (Kniemeyer et al., 2003).
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In addition to sulfate, strain ALDCT could use thiosulfate (10 mM) as an electron acceptor for alkane degradation. Sulfite, elemental sulfur and Fe(III) were not reduced. Strain ALDCT could grow in the basal medium without a vitamin supplement. However, folic acid, cyanocobalamin and thiamine improved growth, as did yeast extract (0.005 %). The DNA G+C content determined by HPLC was 53.6 mol%.
Phylogenetic analysis
Analysis of an almost-complete sequence (1495 bp) of the 16S rRNA gene of strain ALDCT (GenBank accession no. DQ303457) and an almost-complete sequence (1484 bp) of the same gene of strain Lake (DQ303458) revealed that they belonged to the Deltaproteobacteria and were phylogenetically close to each other but not to other known mesophilic, alkane-degrading strains (AK-01, Pnd3, Hxd3 and CV2803T) in the genus Desulfatibacillum (Cravo-Laureau et al., 2004) (Fig. 2). Strains ALDCT and Lake were phylogenetically very closely related (1483/1484 bp; 99.9 % 16S rRNA gene sequence similarity). The 16S rRNA gene sequence similarity to other alkane-degraders that are members of the genus Desulfatibacillum was 88–87 %. The novel strains were most closely related to Desulfacinum species (93–94.7 % similarity) and Syntrophobacter species (91.7–94 % similarity). Maximum-parsimony and maximum-likelihood methods also strongly supported (100 %) a clade consisting of strains ALDCT and Lake, with Syntrophobacter and Desulfacinum as sister clades.
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; Sievert & Kuever, 2000; Rozanova et al., 2001). They can use a broad range of substrates and are able to grow autotrophically with H2. They are capable of growing with long-chain fatty acids. However, the ability to grow with alkanes has never been reported. The genus Syntrophobacter is composed of syntrophic bacteria that can grow by the oxidation of propionate in co-cultures with a H2/formate-utilizing partner. They do not oxidize acetate or other fatty acids. They can grow slowly as pure sulfate-reducing cultures with certain substrates but, to our knowledge, the ability to grow with alkanes either in pure culture or in syntrophic associations has not been reported (McInerney et al., 2005).
The nucleotide sequence difference between strains ALDCT and Lake and the aforementioned taxa is close to the accepted hypothetical sequence similarity value (95–93 %) for differentiating between genera (Fry et al., 1991; Mullins et al., 1995; Sheridan et al., 2003). This distinction, in combination with the physiological differences and the fact that no members of Desulfacinum or Syntrophobacter have been reported to degrade n-alkanes, argues against the allocation of strain ALDCT within either of these genera. Based on physiological characteristics and phylogenetic relationships with other Deltaproteobacteria, we propose that strain ALDCT represents a novel species in a new genus, Desulfoglaeba alkanexedens gen. nov., sp. nov. Strain Lake, which is closely related to strain ALDCT but was isolated from a different location, may represent another member of this new genus. Additional physiological details are required for accurate determination of its status.
Description of Desulfoglaeba gen. nov.
Desulfoglaeba (De.sul.fo.glae'ba. L. prep. de from; N.L. sulfo used for fem. n. sulfas sulfate in genus names of sulfate-reducing prokaryotes; L. fem. n. glaeba clump/crumb/aggregate; N.L. fem. n. Desulfoglaeba sulfate-reducing clump/aggregate).
Mesophilic, sulfate-reducing bacteria that tend to form clusters. Cells are oval rods with refractile cores. Non-spore-forming. Strictly specialized in their substrate specificity. Oxidize alkanes completely. The type species is Desulfoglaeba alkanexedens.
Description of Desulfoglaeba alkanexedens sp. nov.
Desulfoglaeba alkanexedens (al.kan.ex.e'dens. N.L. n. alkanum alkane; L. part. adj. exedens eating up; N.L. part. adj. alkanexedens eating up alkanes).
Exhibits the following properties in addition to those given in the genus description. Cells are slightly curved, short rods with oval ends (2.5–3.0x1.0–1.4 µm), often occurring in pairs. Tends to form aggregates or large clusters. Growth occurs at 17–50 °C (optimum 31–37 °C) and pH 4.5–8.2 (optimum 6.5–7.2). NaCl is not required for growth but salt concentrations up to 55 g l–1 can be tolerated. Sulfate and thiosulfate are used as electron acceptors. Alkanes (C6–C12), pyruvate, butyrate, hexanoic acid and 4-methyloctanoic acid can be used as electron donors. Vitamins are not required, but folic acid, cyanocobalamin (vitamin B12) and thiamine improve growth. Yeast extract in low concentrations (0.005 %) stimulates growth.
The DNA G+C content of the type strain is 53.6 mol%. The type strain, ALDCT (=JCM 13588T=ATCC BAA-1302T), was isolated from oily sludge collected from a naval wastewater-storage facility at the US Navy Craney Island Fuel Depot in Portsmouth, VA, USA.
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ACKNOWLEDGEMENTS |
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