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1 National Space Sciences and Technology Center/NASA, XD-12, 320 Sparkman Dr., Astrobiology Laboratory, Huntsville, AL 35805, USA
2 Japan Collection of Microorganisms, RIKEN BioResource Center, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan
3 American Type Culture Collection, 10801 University Blvd, Manassas, VA 20110, USA
4 United States Department of Agriculture, Monitoring Programs Office, 8609 Sudley Rd, suite 206, Manassas, VA 20110, USA
5 Department of Microbiology, University of Georgia, Athens, GA 30602-2605, USA
Correspondence
Elena V. Pikuta
elenapikuta{at}hotmail.com
Richard B. Hoover
Richard.Hoover{at}NASA.GOV
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9c and C16 : 0. 16S rRNA gene sequence analysis of strain SCAT showed a similarity of approximately 97 % with the type strains of Clostridium formicaceticum and Clostridium aceticum in clostridial cluster XI and a similarity of less than 94.2 % to any other recognized Clostridium species and those of related genera in this cluster. Strain SCAT was clearly differentiated from C. formicaceticum and C. aceticum based on comparison of their phenotypic properties and fatty acid profiles, as well as low levels of DNA–DNA relatedness between strain SCAT and the type strains of these two species. Therefore, strain SCAT is considered to represent a novel species of a new genus, Anaerovirgula multivorans gen. nov., sp. nov., in clostridial cluster XI. The type strain is SCAT (=ATCC BAA-1084T=JCM 12857T=DSM 17722T=CIP 107910T).
Images of cells of strain SCAT and graphs showing growth of the strain under varying salinity, pH and temperature conditions are available as supplementary material in IJSEM Online.
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). In our laboratory, the process of cellulose degradation was studied with anaerobic sediments from alkaline Owens Lake, California, USA. At room temperature, a piece of filter paper was completely dissolved over a period of 7–10 days. The dominant bacterial forms observed microscopically were motile rods and spirochaetes (Pikuta et al., 2005). Subsequent isolation of both of these morphotypes led to the characterization of two saccharolytic strains, SCAT and ASpC2T. The study showed that in addition to the hydrolysis of cellulose, strain ASpC2T was able to ferment sugars, but strain SCAT exhibited a much broader fermentative metabolism; it fermented sugars, some organic acids, amino acids and proteolysis products. In pure or binary cultures, these isolates exhibited a weak ability to hydrolyse cellulose, but only in the presence of yeast extract. Here we present a taxonomic description of the obligately anaerobic strain SCAT which, based on its phenotypic and genotypic features, is considered to represent a novel species of a new genus within clostridial cluster XI.
Black mud sediments with a pH of 10.0 and a strong smell of hydrogen sulfide were collected anaerobically from beneath shallow water (temperature 30 °C, salinity 3 %) on the eastern side of Owens Lake in August 2000. Sampling, maintenance, transportation and storage were as previously described by Hoover et al. (2003) and Pikuta et al. (2003a). Enrichment cultures were obtained using an anaerobic technique and the medium contained (per litre): 30 g NaCl, 2.76 g Na2CO3, 24.0 g NaHCO3, 0.2 g KCl, 0.2 g K2HPO, 0.1 g MgCl2.6H2O, 1.0 g NH4Cl, 0.4 g Na2S.9H2O, 0.001 g resazurin, 0.1 g yeast extract, 2 ml vitamin solution (Wolin et al., 1963) and 1 ml trace mineral solution (Whitman et al., 1982); the final pH was adjusted to 9.5. Filter paper or microcrystalline cellulose (5 g l–1; Sigma) was used as the substrate. The gas phase was composed of high-purity nitrogen gas. Serial dilutions were performed in Hungate tubes with a filter paper substrate. Cultures on the 10–9 dilution with one morphotype observed microscopically were chosen for subsequent ‘roll-tube’ serial dilution purification. Upon inoculation of ‘roll-tubes' containing a medium with 3 % (w/v) agar and D-glucose, colonies appeared after 3–4 days incubation at 35 °C. These colonies were white to yellowish-cream in colour and were round to convex lens shaped (in deep agar) with a diameter of 0.5–1.3 mm. The colonies were also circular with smooth, thin edges and a darker coloured centre that had a denser consistency. One of the colonies from the 10–9 dilution was chosen as the type strain and was designated SCAT. Unless specified otherwise, all subsequent incubations were performed at 35–37 °C. During the substrate utilization tests, the purity of the culture was checked by reverse inoculation to the first substrate. The culture purity was also routinely monitored microscopically.
Cell morphology of the novel isolate was examined under a Fisher Micromaster phase-contrast microscope. Cells of strain SCAT were long, straight rods with rounded ends and ranged from 0.4 to 0.5 µm in width and from 2.5 to 5.0 µm in length. Cells were motile and Gram-positive. Spores were round and located terminally without swelling sporangium. Cells occurred singly, in pairs or in short slightly curved chains. Images of cells of strain SCAT viewed with an Olympus BX41 light microscope equipped with a CytoViva 150 Illumination System (Vodyanoy, 2005) are available as Supplementary Fig. S1 in IJSEM Online.
Growth of the culture was determined by direct cell counting under a microscope or by measuring the optical density at 595 nm (Genesis 5; Spectronic Instruments). Catalase activity was determined based on the reaction with hydrogen peroxide (Gerhardt et al., 1994). Substrates were added to the medium at concentrations of 3 g l–1. The medium also contained 0.1 g yeast extract l–1. Gases were measured using a Varian 3700 gas chromatograph equipped with a Porapak Q column and thermal conductivity/flame ionization detector. Nitrogen was used as the gas carrier.
The novel isolate was an obligate anaerobe and grew exclusively under anaerobic conditions. Strain SCAT was catalase-negative. It was obligately dependent upon Na+ ions and could not grow without NaCl (the experiment was performed on medium in which all sodium salts were substituted by potassium salts and all Cl–-containing salts were replaced by 
salts). At a concentration of 0.5 % (w/v) NaCl, growth was observed after a significantly longer lag phase than at optimal growth conditions. Optimum growth was at 1 % NaCl on the medium for which the total salinity (with carbonate and bicarbonate salts) was 2 % (w/v). The NaCl range for growth was 0.5–9.0 % (w/v) (see Supplementary Fig. S2 in IJSEM Online). No growth was observed within 60 days at 0 or 10 % NaCl. At 1 % NaCl, strain SCAT grew in the pH range from 6.7 to 10.0, with optimum growth at pH 8.5 (see Supplementary Fig. S2). At a salt concentration of 3 % NaCl and 1 % other salts in the test medium, strain SCAT grew at pH 7.5, but not at pH 7.0. In a medium without carbonate-containing salts at pH 7.5 (a medium used routinely for the growth of neutrophilic bacteria), growth was very poor; cell yield was low and extensive spore formation was observed, confirming that the novel isolate was truly alkaliphilic. Growth was not dependent on CO3 ions; good growth was observed on glycine-buffered medium at pH 9.0 without carbonate-containing salts (three subsequent passages demonstrated good growth). Strain SCAT was mesophilic. Growth was observed at 10–45 °C, with optimal growth at 35 °C (Supplementary Fig. S2 in IJSEM Online).
Strain SCAT had a chemo-organoheterotrophic metabolism and was capable of growth on a range of substrates (see Table 1 and the species description below). Growth on cellulose and filter paper was slow and weak and required 0.1 g yeast extract l–1; filter paper was never completely hydrolysed. Hence strain SCAT could be considered as a facultatively cellulolytic bacterium.
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Antibiotic inhibition was tested at a concentration of 250 µg ml–1 (except for chloramphenicol, which was tested at 125 µg ml–1) and the results are given in the species description. Growth with ampicillin exhibited a prolonged lag phase (3–4 days).
For extraction of fatty acid methyl esters, strain SCAT was incubated for 4 days at 22 °C on the medium described above (with D-fructose as a substrate). Other reference strains (Clostridium formicaceticum ATCC 27076T and Clostridium aceticum ATCC 35044T) received from the ATCC for comparative study were incubated at the same conditions on ATCC 1612 medium, which is very close in composition to that used for the novel isolate. The extraction and analysis procedures were as described previously (Pikuta et al., 2003b). The major fatty acids of strain SCAT were C14 : 0, iso-C15 : 0, C16 : 19c and C16 : 0, whereas those of the two reference strains were C14 : 0, C16 : 19c and C16 : 0 (no iso-C15 : 0; Table 2).
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, except that 2 units of S1 nuclease were used instead of P1 nuclease and the nuclease degradation was performed in a 20 mM sodium acetate buffer, pH 5.0. The total G+C content of the purified genomic DNA for strain SCAT was 34.2±0.2 mol% (mean±SD, n=12).
For 16S rRNA gene sequence analysis, cells were lysed by sonication and the genomic DNA was isolated following phenol/chloroform extraction and ethanol precipitation (Sambrook et al., 1989). The 16S rRNA genes were PCR amplified with primers EB-10F (5'-AGTTTGATCCTGGCTC, positions 10–25 according to the Escherichia coli numbering system) and EB-1530R (5'-AAGGAGGTGATCCAGCC, positions 1541–1525).
The amplified 16S rRNA genes were sequenced directly in an ABI PRISM 310 Genetic Analyser (Applied Biosystems) with the 16S rRNA internal primers (Namwong et al., 2005). In addition, to confirm the sequence of both end regions, the product purified by recovery from agarose gels using a GenElute Minus EtBr spin column (Sigma) was cloned into pT7 Blue vectors (Novagene), transformed in competent cells (E. coli JCM 109) and the plasmid DNAs were sequenced with the vector primers. Multiple alignments of the sequence were performed with CLUSTAL X (Thompson et al., 1997). The alignment was manually verified and edited. After gaps and ambiguous bases were eliminated, evolutionary distances were calculated (see below) and a phylogenetic tree (Fig. 1) was constructed by using the neighbour-joining method (Saitou & Nei, 1987). Confidence values of branches of the phylogenetic tree were determined using bootstrap analyses (Felsenstein, 1985) based on 1000 resamplings.
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). The phylogenetic tree was constructed with representative strains of clostridial cluster XI by comparing 1202 nucleotide positions as shown in Fig. 1
. Strain SCAT formed a cluster with the type strains of C. aceticum and C. formicaceticum, with sequence similarity values, based on pairwise comparison, of 97.0 % (1479 positions) and 96.6 % (1366 positions), respectively. Strain SCAT was distantly related to other members of clostridial cluster XI (<94.2 % 16S rRNA gene sequence similarity).
DNA–DNA hybridization studies, performed according to the method of Ezaki et al. (1989), revealed that strain SCAT was not a member of either of these two species, showing low hybridization values to C. formicaceticum ATCC 27076T and C. aceticum ATCC 35044T (13 and 11 %, respectively).
Strain SCAT was isolated from a sample of anaerobic sediments of soda Owens Lake, which is a highly alkaline, evaporitic, carbonate-saturated lake remnant that has undergone the complete cycle of synthesis and degradation of organic matter. Photosynthetic prokaryotes (cyanobacteria and purple bacteria linked to the sulfur cycle) represent the primary producers of organic matter in the lake; the decomposers are represented by cellulolytic, sugarlytic, proteolytic, bacteriolytic, sulfate-reducers, together with other secondary anaerobes (Pikuta et al., 2005).
The novel isolate occurs within a group of obligately anaerobic, alkalitolerant and alkaliphilic species of clostridial cluster XI. The role of this novel bacterium within the community studied is polyfunctional. The organism participates in cellulose decomposition as a primary anaerobe, it also performs hydrolysis of bimeric and monomeric sugars and products of proteolysis as a dissipotroph and finally it performs the role of a secondary anaerobe by using low-energy molecules of organic acids such as lactic, pyruvic and citric acid.
While this paper was in preparation, the anaerobic, alkaliphilic bacterium Clostridium alkalicellulosi Z-7026T (capable of growing exclusively on cellulose, xylan and cellobiose) was described by Zhilina et al. (2005). This bacterium belongs to clostridial cluster III. This highly specialized cellulose- and xylan-decomposer is incapable of fermenting monosaccharides, disaccharides other than cellobiose, other polymeric sugars or proteins. These properties are quite different from those of strain SCAT.
It is interesting that strain SCAT is capable of growth on L-isomers of sugars, which suggests the possible presence of alkaliphilic isomerases in its metabolism. The distinguishing features of the novel isolate and closely related species C. formicaceticum and C. aceticum are shown in Table 1. Phenotypic differences between the novel isolate and C. formicaceticum ATCC 27076T are as follows: cell size (diameter of cells of strain SCAT is three times smaller), ability to ferment D-glucose, sucrose, D-mannitol, methanol and lactate. Furthermore, C. aceticum ATCC 35044T is a classical homoacetogen that is capable of growth on H2+CO2, but strain SCAT cannot grow on hydrogen or H2+CO2 and the G+C content of the genomic DNA is different by 1 mol%.
The fatty acid content of strain SCAT is also very different from that of the two phylogenetically closest related species. The C14 : 0 fatty acid content of strain SCAT is less than half that of C. formicaceticum ATCC 27076T and C. aceticum ATCC 35044T, and strain SCAT contains only one-third the content of C16 : 0 aldehydes present in the latter two strains. Finally, iso-branched fatty acids are abundant in strain SCAT (24.0 % in total), but completely absent in the other two organisms (Table 2).
Strain SCAT can also be differentiated from recognized genera in clostridial cluster XI, such as Natroninocola, Tindallia, Alkaliphilus and Caminicella, with less than 94.2 % 16S rRNA sequence similarity to the type species of these genera. In addition to its phylogenetic distinctiveness, strain SCAT can be differentiated from these non-Clostridium genera based on its phenotypic properties (Table 3). Members of the genus Natronincola are halophilic (>4 %) and do not ferment sugars; representatives of the genus Tindallia have higher genomic DNA G+C contents and no iso-C15 fatty acids and species of the genus Alkaliphilus have less C16 : 1 fatty acid methyl esters. On the basis of these data, strain SCAT should be classified in a new genus in clostridial cluster XI.
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). Thus, strain SCAT (as well as C. formicaceticum and C. aceticum) should in principle be accommodated within a separate new genus. However, given the differences in metabolism, low DNA–DNA relatedness value and the significantly different fatty acid profiles, we do not consider it appropriate at this time to move the latter two species to a new genus. Further comparative studies will need to be carried out to clarify the taxonomic status of C. formicaceticum and C. aceticum, which may subsequently be reclassified and included in the new genus Anaerovirgula. On the basis of phenotypic and genotypic characteristics, including Gram-positive cell walls, spore formation, obligately anaerobic and fermentative metabolism, mesophilic and alkaliphilic physiology, dependence on NaCl for growth, fatty acid content, 16S rRNA gene sequence divergence and levels of DNA–DNA relatedness, strain SCAT is proposed as the type strain of a novel species in a new genus, Anaerovirgula multivorans gen. nov., sp. nov.
Description of Anaerovirgula gen. nov.
Anaerovirgula (An.aer.o.vir'gu.la. Gr. pref. an not; Gr. n. aer aeros, air; L. fem. n. virgula a small rod; N.L. fem. n. Anaerovirgula an anaerobic small rod).
Gram-positive, spore-forming, small (2.5–5.0 µm) rod-shaped cells that occur alone, in pairs or in short chains. Obligately anaerobic, and catalase-negative. Alkaliphilic and mesophilic. Chemo-organotrophic, with a fermentative metabolism (sugars and proteolysis products) and capable of respiration by the Stickland reaction. The fatty acid profile differs from that of members of the same clostridial cluster in the following respects: presence of iso-C15 : 0 fatty acid methyl esters, reduced quantity of C14 : 0 fatty acid methyl esters and significantly reduced quantity of C16 : 0 aldehydes. The G+C content of the genomic DNA is around 34 mol%. Belongs to clostridial cluster XI as defined by Collins et al. (1994).
The type and only species is Anaerovirgula multivorans.
Description of Anaerovirgula multivorans sp. nov.
Anaerovirgula multivorans (mul.ti.vo'rans. L. adj. multus many; L. part. adj. vorans devouring; N.L. part. adj. multivorans devouring numerous kinds of substrates).
Cells are motile, straight rods with rounded ends, 0.4–0.5x2.5–5.0 µm in size. Spores are terminally located. Growth occurs between 10 and 45 °C (optimum 35 °C), and at pH22 °C 6.7–10.0 (optimum pH 8.5). Range of NaCl for growth is 0.5–9 % (w/v), with optimum growth at 1–2 % (w/v) NaCl. Heterotrophic growth occurs with lactate, pyruvate, citrate, glycerol, D-mannitol, D-glucose, D-fructose, D-maltose, D-trehalose, D-ribose, L-ribose, L-arabinose, sucrose, pectin, starch, D-cellobiose, cellulose, filter paper, triethylamine, peptone, yeast extract, Casamino acids, chitin, L-cysteine, L-aspartic acid, L-arginine, L-histidine, trans-4-hydroxy-L-proline, L-serine, L-alanine, L-lysine and L-glutamine. No growth on H2+CO2, H2 alone, formate, acetate, propionate, butyrate, acetone, ethanol, methanol, lactose, D-arabinose, L-mannose, L-glucose, D-fucose, L-fucose, betaine, trimethylamine, D-arginine, L-proline, D-proline, D-lysine, D-serine, glycine, L-tyrosine, L-threonine, D-threonine, L-cystine or L-valine. Produces CO2 but not H2 during fermentation. Capable of respiration by the Stickland reaction on the following amino acid pairs: L-proline+L-isoleucine and L-proline+L-leucine. No growth on L-proline+L-valine, glycine+L-leucine, glycine+L-isoleucine, glycine+L-valine or L-tryptophan+L-valine. Resistant to ampicillin and kanamycin, but sensitive to gentamicin, tetracycline, rifampicin and chloramphenicol. The G+C content of the genomic DNA is 34.2 mol%.
The type strain, SCAT (=ATCC BAA-1084T=JCM 12857T=DSM 17722T=CIP 107910T), was isolated from anaerobic, alkaline mud sediments of Owens Lake, California, USA.
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ACKNOWLEDGEMENTS |
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