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School of Life Sciences, Arizona State University, Main Campus, Tempe, AZ 85287-4501, USA
Correspondence
Ferran Garcia-Pichel
ferran{at}asu.edu
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ABSTRACT |
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7c and C16 : 0. It had a high DNA G+C content of 75 mol%. Comparisons of 16S rRNA gene sequences identified bacteriochlorophyll a-producing strains of Paracraurococcus ruber (94·9 %), Craurococcus roseus (92·2 %) and Roseococcus thiosulfatophilus (92·3 %), as well as non-bacteriochlorophyll a-producing bacteria Muricoccus roseus (94·9 %), Roseomonas gilardii (94·2 %) and Roseomonas mucosa (93·8 %), as the bacteria most closely related to strain CP2CT. Phylogenetically, CP2CT was placed roughly equidistantly from the above organisms. Based on its phylogenetic placement and morphological and physiological characteristics, strain CP2CT is assigned to a new genus in the 
-1 subgroup of the Proteobacteria, for which the name Belnapia gen. nov. is proposed. Strain CP2CT (=ATCC BAA-1043T=DSM 16746T) is proposed as the type strain of the type species of this genus, with the name Belnapia moabensis gen. nov., sp. nov.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain CP2CT is AJ871428.
A 16S rRNA gene sequence similarity matrix, a comparison of nucleotides in the 16S rRNA gene sequence between Belnapia moabensis and related species and UPGMA and maximum-parsimony phylogenetic trees are available as supplementary material in IJSEM Online.
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). BSCs are thought to contribute to a number of processes in the environment, especially to those that occur at the land surface or soil–air interface. These include soil stability, erosion resistance, atmospheric N2 fixation, nutrient contributions to plants, soil–plant–water relations, infiltration, seedling germination and plant growth (Belnap & Gardner, 1993; Belnap, 2002; Johnson et al., 2005). They are particularly common in semiarid and arid environments throughout the world (Belnap, 1994). BSCs are dominated by cyanobacteria, lichens and sometimes by mosses or eukaryotic algae as primary producers (Belnap et al., 2001). Bacteria and fungi are the major heterotrophic components, but little is known about their taxonomic placement. Recent survey studies from various geographical settings (L. M. Nagy, P. Alejandro and F. Garcia-Pichel, unpublished; G. S. N. Reddy and F. Garcia-Pichel, unpublished; Smith et al., 2004) point to the dominance of poorly known and probably novel taxa of Actinobacteria, Proteobacteria, ‘Bacteroidetes’ and low-DNA G+C-content Gram-positive bacteria. Attempts at cultivation and characterization of these bacteria are limited to Dyadobacter crusticola, belonging to the ‘Bacteroidetes’ (Reddy & Garcia-Pichel, 2005). In the present study, we characterized a BSC isolate belonging to the Alphaproteobacteria using polyphasic taxonomic methods. The phenotypic, chemotaxonomic and phylogenetic analyses established that the isolate does not belong to any of the genera described so far. Therefore, it was classified under a new genus, Belnapia gen. nov., with the name Belnapia moabensis sp. nov.
Strain CP2CT was isolated from a BSC sample near the town of Moab (UT, USA), in the Colorado Plateau (38° 34' 984'' N and 109° 31' 451'' W; collected between 20 and 22 May 2003). The physico-chemical characteristics of the sampling site have been described by Garcia-Pichel et al. (2003) and Johnson et al. (2005). Initially, a 0·5 g sample was suspended in Ringer's solution (9 g NaCl, 0·042 g KCl, 0·025 g CaCl2 and 100 ml distilled water) and shaken for 30 min. The suspension was allowed to settle and 100 µl supernatant was plated on PGY-BG11 agar (Reddy & Garcia-Pichel, 2005) and incubated in the dark at room temperature. A red-pigmented colony was isolated, purified and maintained on PGY-BG11.
Cell morphology was studied using light microscopy and scanning electron microscopy (SEM). For SEM, cells were mounted on Formvar-coated copper grids and negatively stained with 0·5 % (w/v) uranyl acetate. Grids were examined in a JEM-1010 SEM (JEOL) operated at 60 kV. Growth at different temperatures was determined using 10xPGY-BG11 medium. For growth at different pH, the components of 10xPGY-BG11 were dissolved in 0·1 M phosphate buffer with pH values ranging from 5 to 12. Tolerance to salt was observed by the addition of NaCl (0·5–6 %, final concentration) in 10xPGY-BG11. For all biochemical tests, cells were grown on 10xPGY-BG11. Catalase activity was determined by bubble production in 30 % (v/v) aqueous hydrogen peroxide solution. Oxidase activity was tested by oxidation of 1 % (w/v) tetramethyl-p-phenylenediamine (Merck) to a deep purple or blue colour. Nitrate reduction, hydrolysis of aesculin, casein, starch, Tween 80, urea and gelatin and various enzyme activities were determined on 10xPGY-BG11 according to previously described methods (Lanyi, 1987; Smibert & Krieg, 1994). Carbon assimilation tests were performed by adding each carbon compound, at a final concentration of 0·5 %, to a base of BG11 medium lacking citric acid (Reddy & Garcia-Pichel, 2005). Antibiotic susceptibility was assayed with antibiotic discs, according to the Kirby–Bauer method (Becton Dickinson Microbiological systems). For testing aerobic and anaerobic photoautotrophic growth, culture was inoculated into liquid and streaked onto agarized BS-V (Saitoh & Nishimura, 1996) or PNP media at pH 6·8 and incubated in the light at room temperature. PNP contained, (l–1), 0·5 g NaCl, 0·4 g MgCl2.6H2O, 0·1 g CaCl2.2H2O, 0·2 g KH2PO4, 0·05 g KCl, 0·5 g Na2HCO3, 2·38 g HEPES, 1 ml 1000xvitamin solution and 1 ml trace element solution. The vitamin solution contained, (100 ml–1); 5 mg biotin, 100 mg thiamin, 100 mg nicotinic acid, 50 mg p-aminobenzoic acid, 1 mg vitamin B12, 50 mg calcium pantothenate, 50 mg pyridoxine hydrochloride, 50 mg folic acid and 20 mg trisodium EDTA. The composition of the trace element solution used was as follows, (l–1), 10 mg ZnSO4.7H2O, 3 mg MnCl2.4H2O, 30 mg H3BO3, 20 mg CoCl2.6H2O, 1 mg CuCl2.2H2O, 2 mg NiCl2.6H2O and 3 mg Na2MoO4. Anaerobic conditions were achieved in GasPak jars with GasPak Plus anaerobic system envelopes (Becton Dickinson). The head space of the jars contained CO2 and H2. The ability of the culture to fix nitrogen was tested using BG11 medium without nitrate (BG110), but containing 0·5 % glucose (w/v) as the carbon source.
Quantitative analysis of whole-cell fatty acids was performed by growing strain CP2CT on tryptic soy agar medium at 25 °C. Fatty acid methyl esters were prepared according to the instructions for the Microbial Identification System (Microbial ID) and analysed using gas chromatography/mass spectrometry. Lipids were extracted and analysed according to Suresh et al. (2004). Respiratory quinones were extracted and analysed as described by Komagata & Suzuki (1987). For pigment characterization, cells were grown on 10xPGY-BG11 plates, scraped off the surface, suspended in 50 mM phosphate buffer or methanol and sonicated for 10 min at 4 °C. The suspension was centrifuged at 10 000 r.p.m. to remove unbroken cells. Absorption spectra were recorded for the supernatant with a Shimadzu UV-1601 spectrophotometer from 200 to 1100 nm. For in vivo pigment characterization, cells were grown aerobically under dark and light conditions at room temperature, suspended in 50 % glycerol containing 0·04 % sodium thioglycollate (to prevent oxidation of pigments) and the spectrum was recorded using 50 % glycerol containing 0·04 % sodium thioglycollate as a blank (Bryantseva et al., 2000). The pigments were further resolved on HPLC with online diode array detection using a u-Bondapack C18 reverse-phase column. The solvent system employed was a gradient of 1 M ammonium acetate/methanol (1 : 4) (solvent A) to methanol (solvent B). The gradient used was 0 % solvent A at time 0 to 5 min and, at 40 min, 100 % solvent B. The flow rate used was 1 ml min–1 and the detector was set at 519 nm.
DNA was isolated and the G+C content (mol%) was determined according to Reddy et al. (2000). A mean value from two independent experiments was calculated; the variation between the experiments was less than 2 %. PCR amplification of approximately 1·5 kb of the puf gene was achieved and it was sequenced using the primer set PULM1 (5'-KTTCGACTTCTGGGTSGG-3') and PULM2 (5'-CCCATSGTCCAGCGCCAG-3') (Alarico et al., 2002) and a strain of Rhodopseudomonas isolated in our lab was used as a control.
For 16S rRNA gene sequencing, DNA was prepared using the MoBio microbial DNA isolation kit (MoBio Laboratories). Approximately 1·5 kb of the 16S rRNA gene was amplified using primers GM3F (5'-AGAGTTTGATCMTGGC-3'; Nübel et al., 1997) and 16S2 (5'-ACGGCTACCTTGTTACGACTT-3'; Reddy et al., 2000). Fragments of around 1500 bp were purified from agarose gels with a Qiagen kit and sequenced using the primers 907R (5'-CCGTCAATTCCTTTRAGTTT-3'; Nübel et al., 1997), pC* (5'-CCCACTGCTGCCTCCCGTAG-3'), pE (5'-AAACTCAAAGGAATTGACGG-3') and 16S2 (Reddy et al., 2000). The phylogenetic position of CP2CT was ascertained by aligning the partial sequence of the 16S rRNA gene containing 1453 nucleotides [nucleotides 6–1513 according to the Escherichia coli 16S rRNA (J 01695) numbering], with closely related sequences belonging to the Alphaproteobacteria, using the CLUSTAL W program (Thompson et al., 1994). These sequences were included after the initial BLAST search. Pairwise evolutionary distances were computed using the DNADIST program with the Kimura two-parameter model, as developed by Kimura (1980). Phylogenetic trees were constructed using three tree-making algorithms, neighbour-joining, unweighted pair group method with arithmetic averages (UPGMA) and DNA parsimony program (DNAPARS), from the MEGA2 package (Kumar et al., 2001). Clade stability in the phylogenetic tree was assessed by analysing 1000 replicates of the dataset.
Strain CP2CT forms colonies that are 1–2 mm in diameter, convex, rough and red-pigmented with rounded margins. Cells are coccoid, occur singly, in pairs and in groups (Fig. 1a, b) and are non-motile. They are catalase-, oxidase- and urease-positive, have C18 : 17c, C16 : 0, C18 : 1 2-OH and C16 : 17c/C15 : 0 iso 2-OH as the major fatty acids and have a DNA G+C content of 75 mol%. Other characteristics of CP2CT are given in the species description. CP2CT did not grow phototrophically under aerobic or anaerobic conditions on PNP or BS-V media (Saitoh & Nishimura, 1996). Methanolic (Fig. 2) or buffer extracts of the pigments or pigments recorded in vivo did not show any peaks characteristic of bacteriochlorophylls. In addition, PCR amplification of puf genes, using specific primers (Alarico et al., 2002), resulted in no product, indicating that the biosynthetic genes for bacteriochlorophyll a (Bchl a) are absent in CP2CT.
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The 16S rRNA gene sequence of CP2CT contains all of the signature nucleotides that are characteristic of the Alphaproteobacteria and the strain could be grouped in the -1 subgroup (Woese, 1987). A BLAST sequence similarity search, based on the 16S rRNA gene sequence, identified Paracraurococcus ruber (Saitoh et al., 1998), Muricoccus roseus (Kämpfer et al., 2003), Roseomonas gilardii (Rihs et al., 1993), Roseomonas mucosa (Han et al., 2003), Rubritepida flocculans (Alarico et al., 2002) and Roseococcus thiosulfatophilus (Yurkov et al., 1994) as related organisms. The evolutionary distances, calculated using the Kimura-2 factorial model and based on 16S rRNA gene sequences, indicated that CP2CT is related to Pcr. ruber (94·9 %), M. roseus (94·9 %), R. gilardii (94·2 %), R. mucosa (93·8 %), Rsc. thiosulfatophilus (92·3 %), Teichococcus ludipueritiae (92·3 %), Crc. roseus (92·2 %), Rut. flocculans (92·2 %), Rpi. globiformis (91·5 %) and Acidiphilium cryptum (90·7 %) (see Supplementary Table S1 in IJSEM Online). As strain CP2CT exhibited a 16S rRNA gene sequence similarity of less than 97·5 % with all of these closely related species, CP2CT does not represent a novel strain of any of these species (Stackebrandt & Goebel, 1994), but could represent a novel species belonging to one of the genera. A base-to-base comparison of 1447 nucleotides in the 16S rRNA gene sequences of strain CP2CT and its relatives indicated a broad range of nucleotide variation: Pcr. ruber (80), M. roseus (83), R. gilardii (87), R. mucosa (94), Rsc. thiosulfatophilus (112), T. ludipueritiae (112), Crc. roseus (123), Rut. flocculans (120), Rpi. globiformis (137) and A. cryptum (144). In addition, CP2CT exhibited differences of 47 nucleotides (Pcr. ruber) to 55 nucleotides (R. mucosa and T. ludipueritiae) in nucleotides that are highly conserved among these genera. Further, there were 14 nucleotides, T (between 218 and 221), G (382), T (593), G (594), C (647), A (648), A (672), T (1135), G (between 1137 and 1138), A (1141), C (1144), G (1261), A (1267) and T (1276), and three deletions at positions 99, 1010 and after 1463, that are present only in CP2CT (numbering is with respect to the E. coli 16S rRNA gene sequence, J01695) (see Supplementary Table S2 in IJSEM Online). Thus, the phylogenetic signatures suggest that CP2CT can be distinguished at a taxonomic rank higher than species, and probably at the genus level, from the other related species. In fact, some of the above genera have been distinguished mostly on differences at the phylogenetic level. For instance, the genus Paracraurococcus (Saitoh et al., 1998) is phenotypically different from Craurococcus only with respect to maximum growth temperature and hydrolysis of Tween 80 (Saitoh et al., 1998), but it showed sufficient differences in 16S rRNA gene sequence, having a similarity of only 94·7 %, to warrant separation. Similarly, Muricoccus (Kämpfer et al., 2003) was delineated from Roseomonas (Rihs et al., 1993; Han et al., 2003) at a 16S rRNA gene sequence similarity of 95·9 %, though it exhibited differences only with respect to cell shape and fatty acids.
The topology of neighbour-joining and maximum-parsimony trees (Fig. 3 and Supplementary Fig. S1b in IJSEM Online) placed CP2CT roughly equidistant from strains containing BChl a, (Pcr. ruber, Crc. roseus, Rut. flocculans and Rsc. thiosulfatophilus) and lacking BChl a (M. roseus, R. gilardii and R. mucosa). In UPGMA trees (Supplementary Fig. S1a in IJSEM Online), CP2CT clustered with the BChl a-containing Pcr. ruber. The above results clearly indicate that the position of CP2CT is sufficiently distinct and deeply rooted from the strains containing or lacking Bchl a to warrant the creation of a novel genus.
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7c (Table 1). Additional differences are listed in Table 1. Strain CP2CT is also closely related to M. roseus on the basis of rRNA gene sequence similarity (94·9 %; see Supplementary Table S1 in IJSEM Online). Both organisms lack BChl a, but differ in cell morphology (Table 1), a feature sufficient to differentiate them at the genus level (Yoon et al., 2001), and in the lack of lysine decarboxylase, ornithine decarboxylase and arginine dihydrolase activities (Table 1) and C12 : 0 fatty acids. The neighbour-joining tree indicated that CP2CT was most closely related to Rsc. thiosulfatophilus, a result further supported by in-depth 16S rRNA gene sequence comparisons of signature nucleotides (see Supplementary Table S2 in IJSEM Online). However, CP2CT is different from Rsc. thiosulfatophilus in that it is non-motile, does not contain BChl a and is a mesophile (Table 1). CP2CT can be differentiated from the closely related species R. gilardii and R. mucosa on the basis of fatty acid content. CP2CT had the highest DNA G+C content, 75 mol%, of all the bacteria used in the present comparison (which ranged from 61 to 71 mol%). Additional differentiating traits are listed in Table 1.
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). Since CP2CT does not possess the generic characteristics of any of the nine closest genera, we suggest a novel genus to accommodate CP2CT, for which the name Belnapia gen. nov. is proposed. Strain CP2CT represents the type strain of the type species of this genus, Belnapia moabensis sp. nov. Strain CP2CT has several interesting physiological characteristics as it is oligotrophic, salt-sensitive (does not grow in presence of 0·5 % NaCl), grows on 0·5 % phenanthrene and can use oxalate as sole carbon source.
Description of Belnapia gen. nov.
Belnapia (Bel.na'pi.a. N.L. fem. n. Belnapia after J. Belnap, in honour of her contributions to the study of BSCs).
Gram-negative cocci, non-motile, red-pigmented by carotenoids, do not contain Bchl a, aerobic, facultatively fermentative. Positive for catalase, oxidase and urease but test negative for lysine and ornithine decarboxylases and arginine dihydrolase. Do not hydrolyse cellulose or starch. Contain C18 : 17c and C16 : 0 as the major fatty acids, phosphatidylcholine, phosphatidylglycerol and diphosphatidylglycerol (cardiolipin) as polar lipids and ubiquinone-9 as the respiratory quinone. DNA G+C content is 75 mol%. Phylogenetically, a member of the -1 subgroup of the Alphaproteobacteria. The type species is Belnapia moabensis.
Description of Belnapia moabensis sp. nov.
Belnapia moabensis (mo.a.ben'sis. N.L. gen. n. moabensis of Moab, UT, USA, where the type strain was isolated).
Shows the following properties in addition to those given for the genus. Colonies are convex, round and rough. It grows from 15 to 30 °C, but not at 37 °C, with an optimum growth temperature of 25 °C. The pH range for growth is 6–8, with an optimum pH of 7. Cannot tolerate NaCl. Cells test negative for lipase, phosphatase, 
-galactosidase, gelatinase, DNase, arginine decarboxylase and phenylalanine deaminase activities. Negative in methyl red, Voges–Proskauer, indole and Simmons' citrate tests. Does not hydrolyse casein, cellulose, aesculin or starch and does not produce H2S gas, but reduces nitrate to nitrite. Cells do not produce acid from D-fructose, L-arabinose, D-galactose, D-glucose, glycerol, D-maltose, D-mannitol, sucrose, D-sorbitol or D-xylose. Ferments L-arabinose, D-galactose, D-maltose and D-xylose but not D-fructose, D-glucose, lactose, sucrose, D-mannose or D-sorbitol. Utilizes adonitol, D-cellobiose, glucose, dulcitol, fumaric acid, D-glucose, meso-inositol, inulin, lactose, lactic acid, maltose, D-levulose, D-mannitol, D-mannose, D-raffinose, D-ribose, L-rhamnose, L-sorbose, sucrose, D-sorbitol, D-trehalose, D-xylose, L-aspargine, L-isoleucine, L-methionine, L-proline, L-threonine, L-valine, oxalate and phenanthrene as sole carbon sources but not L-arabinose, acetate, citrate, dextran, ethanolamine, D-fructose, fumaric acid, D-galactose, glycerol, D-melibiose, pyruvate, succinate, L-alanine, L-arginine, L-aspartic acid, L-cysteine, L-glycine, L-glutamine, L-glutamic acid, L-histidine, L-leucine, L-lysine, L-phenylalanine, L-serine, L-tryptophan, L-tyrosine, adenine, cytosine, guanine, thymidine, nicotinic acid, tartaric acid or indole. Cells are sensitive to carbencillin (100 µg disc), ceftriaxone (30 µg), chloramphenicol (30 µg), ciprofloxacin (5 µg), doxycycline (30 µg), erythromycin (2 µg), gentamicin (10 µg), novobiocin (30 µg), penicillin (10 U), rifampicin (30 µg), streptomycin (10 µg), sulfisoxazole (300 µg) and sulfathiazole (300 µg), but resistant to aztreonam (30 µg), bacitracin (10 U), cephalothin (30 µg), colistin (10 µg), ethanbutol (50 µg), ethionamide (25 µg), nitrofurantoin (150 µg), polymyxin B (300 U), tetracycline (30 µg), trimethoprim (5 µg) and vancomycin (30 µg). Methanol extracts of the type strain exhibit absorption maxima at 315, 363, 465, 493 and 519 nm. Phosphate buffer suspensions (0·1 M, pH 7·4) absorb maximally at 354, 415, 465, 505 and 536 nm.
The type strain, strain CP2CT (=ATCC BAA-1043T=DSM 16746T), was isolated from a BSC in the Colorado Plateau, USA.
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ACKNOWLEDGEMENTS |
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S. T. Bates, G. S. N. Reddy, and F. Garcia-Pichel Exophiala crusticola anam. nov. (affinity Herpotrichiellaceae), a novel black yeast from biological soil crusts in the Western United States. Int J Syst Evol Microbiol, November 1, 2006; 56(Pt 11): 2697 - 2702. [Abstract] [Full Text] [PDF]
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