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Department of Microbiology, University of Massachusetts, Amherst, MA 01003, USA
Correspondence
Derek R. Lovley
dlovley{at}microbio.umass.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 4 October 2002 as DOI 10.1099/ijs.0.02298-0.
The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain T118T is AF435948.
Present address: GeoSyntec Inc., 629 Massachusetts Avenue, Boxborough, MA 01719, USA. 
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Until recently, there has been much less investigation into the diversity of Fe(III)-reducing micro-organisms than that of micro-organisms carrying out other forms of respiration. However, it is becoming increasingly apparent that there is a wide phylogenetic diversity of Bacteria and Archaea capable of conserving energy to support growth from electron transport to Fe(III) (Lovley, 2000a).
Fe(III)-reducing micro-organisms that can use acetate as an electron donor are of interest because acetate is an important intermediate in the anaerobic degradation of organic matter in sedimentary environments (Lovley & Chapelle, 1995). Micro-organisms capable of oxidizing acetate with the reduction of Fe(III) include Geobacter and Desulfuromonas species within the family Geobacteraceae in the 
-Proteobacteria (Lovley, 2000a), as well as Geothrix fermentans (Coates et al., 1999) and Geovibrio ferrireducens (Caccavo et al., 1996). The Fe(III)-reducing hyperthermophilic Archaea species Geoglobus ahangari (Kashefi et al., 2001) and Ferroglobus placidus (Tor et al., 2001) are also capable of acetate oxidation. These organisms are all strict anaerobes. However, a facultatively anaerobic 
-Proteobacterium capable of acetate oxidation, Pantoea agglomerans SP1, was recently described (Francis et al., 2000).
Most previously studied Fe(III)-reducing micro-organisms have an optimal growth temperature of 20–30 °C, but thermophilic and hyperthermophilic Fe(III)-reducing micro-organisms have also been described (Greene et al., 1997; Kashefi & Lovley, 2000; Lovley, 2000b; Tor et al., 2001; Vargas et al., 1998). There is less information on Fe(III)-reducing micro-organisms growing at lower temperatures, but several psychrophilic enrichment cultures were recently reported to reduce Fe(III) at temperatures as low as 0 °C (Zhang et al., 1999). However, pure cultures of psychrotolerant, Fe(III)-reducing micro-organisms have not previously been reported.
As part of a study to characterize the diversity of metal-reducing micro-organisms in subsurface environments, aquifer material from a Department of Energy subsurface study site in Oyster Bay, VA, USA, was used as an inoculum for the enrichment and isolation of Fe(III)-reducing micro-organisms. Several isolates were obtained from various enrichments. Here we report on one such isolate, which is a novel facultatively anaerobic, acetate-oxidizing, Fe(III)-reducing micro-organism capable of growing at temperatures as low as 4 °C. It is most closely related to micro-organisms in the genus Rhodoferax, but unlike Rhodoferax species, it did not grow as a photosynthetic micro-organism under the experimental conditions provided.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Media and growth conditions.
Techniques for strict anaerobic culture were used throughout. The enrichment medium was a defined freshwater medium (Lovley et al., 1993) that contained 10 mM lactate as the electron donor and 100 mmol l-1 poorly crystalline Fe(III) oxide as the sole electron acceptor. The medium (10 ml) was dispensed in anaerobic pressure tubes and bubbled with N2/CO2 (80 : 20, v/v) to remove dissolved oxygen. The final pH was approximately 6·7. The enrichment culture was initiated with a 1 g sediment inoculum. The cultures were incubated at 20 °C in the dark. Positive Fe(III)-reducing enrichments were transferred (10 % inoculum) at least five times.
To obtain pure-culture isolates, the enrichment was streaked on a similar medium solidified with purified agar (1·5 %) in wide-mouthed glass tubes (Bellco Glass) which were then sealed with a butyl stopper. The slant medium differed in that Fe(III) chelated with nitrilotriacetic acid (NTA) was used in lieu of poorly crystalline Fe(III) oxide. Distinct colonies were picked and restreaked at least three times on solid agar slants, before being suspended in liquid media. Tests for phototrophic growth utilized two different types of medium. The first was a standard phototrophic growth medium adapted from Brock et al. (1994). The second was adapted from the original characterization of the genus Rhodoferax (Hiraishi et al., 1991). Electron donors utilized to test for phototrophic growth included fructose, acetate, hydrogen and succinate.
Characterization of anaerobic growth and electron donor and acceptor utilization.
Cells were incubated at 4 or 25 °C for all growth and donor/acceptor utilization experiments. Cells were enumerated with epifluorescent microscopy (Hobbie et al., 1977). Acetate was quantified by using HPLC. Electron donor utilization was evaluated with 10 mM Fe(III)–NTA as the sole terminal electron acceptor. Lactate and acetate were tested separately as electron donors for studies on the range of electron acceptors reduced. Fe(II) was assayed with ferrozine as described previously (Lovley & Phillips, 1987). Reduction of all other electron acceptors was determined visually by observing precipitation, colour change or turbidity.
Identification of poly-hydroxyalkanoate (PHA) inclusions.
PHA inclusion bodies were identified by staining with Nile blue A, as described by Rees et al. (1992).
16S rDNA and phylogenetic analysis.
Cells grown on lactate and Fe(III)–NTA were collected by centrifugation, and genomic DNA was extracted using the GNOME DNA Isolation Kit (Bio 101). Almost the entire 16S rDNA of strain T118T was amplified using primers 8 Forward (5'-AGAGTTTGATCCTGGCTCAG-3') (Eden et al., 1991) and 1492 Reverse (5'-GGTTACCTTGTTACGACTT-3'). PCR amplification mixtures (total 100 µl) contained 10 µl 10x buffer, 8 µl dNTPs (200 µm), 2 µl BSA (400 ng µl-1), 5 µl DMSO, 3 µl primer, 0·5 µl genomic DNA template and 2·5 U AmpliTaq (PerkinElmer Cetus). Amplification was performed in a PTC-200 Peltier Thermal Cycler (MJ Research) with an initial denaturation step at 96 °C for 2 min, followed by 20 cycles of 95 °C for 30 s, 50 °C for 30 s and 72 °C for 45 s, concluded by a final extension at 72 °C for 10 min. PCR amplification products were prepared for sequencing using a QIAquick PCR Purification kit (Qiagen). DNA sequencing was performed by the Orono DNA Sequencing Facility at the University of Maine. Complete bidirectional sequences were obtained from the PCR amplification product.
The sequences were compared to the GenBank and Ribosomal Database Project (RDP) databases using the BLAST (national center for biotechnology information) and SIMILARITY_RANK (RDP) algorithms. The secondary structure was verified manually. The sequences were aligned with related 16S rDNA sequences from GenBank and the RDP using the Wisconsin Package version 10 sequence editor (Genetics Computer Group). Phylogenetic trees were inferred using the distance, maximum-likelihood and parsimony tools of PAUP* (Swofford, 1998).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Cells that grew in this medium were short, straight, motile rods, approximately 3–5 µm long and 1 µm wide (Fig. 1). All cells had a single, polar flagellum (Fig. 1). Cells stained Gram-negative during all growth phases, and did not form visible spores under any of the growth conditions tested. However, cells in carbon-rich medium did produce inclusion bodies that were apparent under phase-contrast and electron microscopy. These inclusions were later identified as PHA by staining with Nile blue A and imaging with UV light, as described by Rees et al. (1992).
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). Fe(III)–NTA reduction was accompanied by an increase in cell number and a loss of acetate (Fig. 2). The stoichiometry of acetate consumption and Fe(III) reduction was consistent with the metabolism of acetate according to the reaction:
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T118T is only the second facultatively anaerobic micro-organism known to oxidize acetate with the reduction of Fe(III), the first being ‘Shewanella saccharophilia’ strain GC-29 (Coates et al., 1998). It is the first facultatively anaerobic organism found to use benzoate as an electron donor for Fe(III) reduction. Strain T118T is unusual amongst Fe(III)-reducing micro-organisms in its inability to reduce AQDS, as most Fe(III)-reducing micro-organisms, including hyperthermophilic Archaea species, can use this electron acceptor (Lovley, 2000a; Lovley et al., 1996, 1998, 2000).
Temperature optimum and growth at 4 °C
The optimum growth temperature for strain T118T was 25 °C (Fig. 3), but in long-term incubations, there was significant growth at temperatures as low as 4 °C (Fig. 4). Fe(III)-reducers capable of growth at such low temperatures have a competitive advantage in cold, Fe(III)-rich subsurface environments. Far northern aquifers and permafrost areas have sediment temperatures that remain at 0–8 °C (Zhang et al., 1999). Fe(III)-reducing enrichment cultures from marine sediment and Alaskan tundra permafrost reduced Fe(III) faster at 10 °C than at 25 °C, indicating that some organisms may prefer cold temperatures for Fe(III) reduction (Zhang et al., 1999). However, strain T118T is only psychrotolerant, not psychrophilic.
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). Neither the morphology nor the physiology of strain T118T is consistent with the genus Aquaspirillum (Eden et al., 1991). Although strain T118T is morphologically similar to previously described Rhodoferax species, these other species are not reported to grow via anaerobic respiration. Furthermore, strain T118T did not grow phototrophically under conditions that support the growth of Rhodoferax species, nor could it ferment fructose, as has been reported in both Rhodoferax species that have been characterized to date (Hiraishi et al., 1991; Madigan et al., 2000). These physiological and phylogenetic differences are significant enough to warrant placing strain T118T as a novel species within the genus Rhodoferax. The proposed name is Rhodoferax ferrireducens sp. nov.
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Cells are Gram-negative, short rods, 3–5 µm long by 1 µm wide, that are motile via a single polar flagellum. Colonies are glossy white, smooth, round and convex. Optimum temperature and pH are 25 °C and 7·0, respectively. Grows at and reduces Fe(III) at temperatures as low as 4 °C. There is no fermentative or phototrophic growth. Facultatively anaerobic: respires with Fe(III)–NTA, Mn(IV) oxide, fumarate, nitrate and atmospheric oxygen. AQDS, chromium(VI), cobalt-EDTA, elemental sulfur, poorly crystalline Fe(III) oxide, Fe(III) citrate, nitrite, 1 % oxygen, selenate, selenite, sulfate, sulfite, thiosulfate and uranium(VI) are not reduced. Electron donors that are utilized include acetate, lactate, malate, propionate, pyruvate, benzoate and succinate. Does not utilize butanol, butyrate, caproate, ethanol, formate, glycerol, hydrogen, isobutyrate, methanol, propanol or valerate. PHA inclusion bodies fluoresce under UV light when stained with Nile blue A.
The type strain is T118T (=ATCC BAA-621T=DSM 15236T). Isolated from coastal aquifer sediment in Oyster Bay, VA, USA.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Caccavo, F., Jr, Coates, J. D., Rosselló-Mora, R. A., Ludwig, W., Schleifer, K. H., Lovley, D. R. & McInerney, M. J. (1996). Geovibrio ferrireducens, a phylogenetically distinct dissimilatory Fe(III)-reducing bacterium. Arch Microbiol 165, 370–376.[CrossRef][Medline]
Coates, J. D., Councell, T. B., Ellis, D. J. & Lovley, D. R. (1998). Carbohydrate oxidation coupled to Fe(III) reduction, a novel form of anaerobic metabolism. Anaerobe 4, 277–282.
Coates, J. D., Ellis, D. J., Gaw, C. V. & Lovley, D. R. (1999). Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Bacteriol 49, 1615–1622.
Eden, P. E., Schmidt, T. M., Blakemore, R. P. & Pace, N. R. (1991). Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int J Syst Bacteriol 41, 324–325.
Francis, C. A., Obraztsova, A. Y. & Tebo, B. M. (2000). Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1. Appl Environ Microbiol 66, 543–548.
Greene, A. C., Patel, B. K. C. & Sheehy, A. J. (1997). Deferribacter thermophilus gen. nov., sp. nov., a novel thermophilic manganese- and iron-reducing bacterium isolated from a petroleum reservoir. Int J Syst Bacteriol 47, 505–509.
Hiraishi, A., Hoshino, Y. & Satoh, T. (1991). Rhodoferax fermentans gen. nov., sp. nov., a phototrophic purple nonsulfur bacterium previously referred to as the "Rhodocyclus gelatinosus-like" group. Arch Microbiol 155, 330–336.
Hobbie, J. E., Daley, R. J. & Jasper, S. (1977). Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33, 1225–1228.
Kashefi, K. & Lovley, D. R. (2000). Reduction of Fe(III), Mn(IV), and toxic metals at 100 °C by Pyrobaculum islandicum. Appl Environ Microbiol 66, 1050–1056.
Kashefi, K., Tor, J. M., Holmes, D. E., Gaw Van Praagh, C. V., Reysenbach, A.-L. & Lovley, D. R. (2002). Geoglobus ahangari gen. nov., sp. nov., a novel hyperthermophilic archaeon capable of oxidizing organic acids and growing autotrophically on hydrogen with Fe(III) serving as the sole electron acceptor. Int J Syst Evol Microbiol 52, 719–728.[Abstract]
Lovley, D. R. (2000a). Dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. In The Prokaryotes. Edited by M. Dworkin, S. Falkow, E. Rosenberg & E. Stackebrandt. New York: Springer.
Lovley, D. R. (2000b). Fe(III) and Mn(IV) reduction. In Environmental Microbe-Metal Interactions. Edited by D. R. Lovley. Washington, DC: American Society for Microbiology.
Lovley, D. R. & Phillips, E. J. P. (1987). Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53, 1536–1540.
Lovley, D. R. & Chapelle, F. H. (1995). Deep subsurface microbial processes. Rev Geophys 33, 365–381.
Lovley, D. R., Giovannoni, S. J., White, D. C., Champine, J. E., Philips, E. J. P., Gorby, Y. A. & Goodwin, S. (1993). Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159, 336–344.[CrossRef][Medline]
Lovley, D. R., Coates, J. D., Blunt-Harris, E. L., Phillips, E. J. P. & Woodward, J. C. (1996). Humic substances as electron acceptors for microbial respiration. Nature 382, 445–448.[CrossRef]
Lovley, D. R., Fraga, J. L., Blunt-Harris, E. L., Hayes, L. A., Phillips, E. J. P. & Coates, J. D. (1998). Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim Hydrobiol 26, 152–157.[CrossRef]
Lovley, D. R., Kashefi, K., Vargas, M., Tor, J. M. & Blunt-Harris., E. L. (2000). Reduction of humic substances and Fe(III) by hyperthermophilic microorganisms. Chem Geol 169, 289–298.[CrossRef]
Madigan, M. T., Jung, D. O., Woese, C. R. & Achenbach, L. A. (2000). Rhodoferax antarcticus sp. nov., a moderately psychrophilic purple nonsulfur bacterium isolated from an Antarctic microbial mat. Arch Microbiol 173, 269–277.[CrossRef][Medline]
Rees, G. N., Vasiliadis, G., May, J. W. & Bayly, R. C. (1992). Differentiation of polyphosphate and poly-
-hydroxybutyrate granules in an Acinetobacter sp. isolated from activated sludge. FEMS Microbiol Lett 94, 171–173.
Swofford, D. L. (1998). PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods) Sunderland, MA: Sinauer Associates.
Tor, J. M., Kashefi, K. & Lovley, D. R. (2001). Acetate oxidation coupled to Fe(III) reduction in hyperthermophilic microorganisms. Appl Environ Microbiol 67, 1363–1365.
Vargas, M., Kashefi, K., Blunt-Harris, E. L. & Lovley, D. R. (1998). Microbiological evidence for Fe(III) reduction on early earth. Nature 395, 65–67.
Zhang, C., Stapleton, R. D., Zhou, J., Palumbo, A. V. & Phelps, T. J. (1999). Iron reduction by psychrotrophic enrichment cultures. FEMS Microbiol Ecol 30, 367–371.[CrossRef][Medline]
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, Fe(II) with acetate; 
, Fe(II) without acetate; 
, cell density with acetate; 
, cell density without acetate; 
, acetate. Results are the means of triplicate analyses. Error bars represent one standard deviation.
, 25 °C; 
, 30 °C; 
, 37 °C; 
