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1 Immunopathogenesis Section, Laboratory of Clinical Infectious Diseases, National Institute of Allergy and Infectious Diseases, US Department of Health and Human Services, Bethesda, MD 20892, USA
2 Research Technologies Section, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, US Department of Health and Human Services, Hamilton, MT 59840, USA
3 Microbiology Service, Department of Laboratory Medicine, Clinical Center, National Institutes of Health, US Department of Health and Human Services, Bethesda, MD 20892, USA
Correspondence
David E. Greenberg
degreenberg{at}niaid.nih.gov
| ABSTRACT |
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7c) and C16 : 0. The DNA base composition was 59.1 mol% G+C. The very weak production of acetic acid from ethanol, the ability to use methanol, the yellow pigmentation and high optimum temperature for growth distinguished this organism from other acetic acid bacteria. The unique phylogenetic and phenotypic characteristics suggest that the bacterium should be classified within a separate genus, for which the name Granulibacter bethesdensis gen. nov., sp. nov. is proposed. The type strain is CGDNIH1T (=ATCC BAA-1260T=DSM 17861T).
The GenBank/EMBL/DDBJ accession number for the 16S rRNA, ITS and recA gene sequences of strain CGDNIH1T are AY788950, DQ340304 and DQ340305, respectively.
A percentage similarity table of the ITS region and a phylogenetic tree based on RecA protein analysis are available as supplementary material in IJSEM Online.
These authors contributed equally to this work. ![]()
| MAIN TEXT |
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Chronic granulomatous disease (CGD) is a rare inherited disease of the phagocyte NADPH oxidase system, which leads to defective production of superoxide and hydrogen peroxide (Segal et al., 2000
). Patients suffer from recurrent life-threatening infections with catalase-producing organisms and also develop tissue granulomas (Winkelstein et al., 2000
). Organisms typically associated with CGD infection include members of the genera Staphylococcus, Serratia, Burkholderia, Nocardia and Aspergillus (Dorman et al., 2002
; Guide et al., 2003
; Speert et al., 1994
). In August 2003, a novel Gram-negative rod was isolated from cervical and supraclavicular lymph nodes of a CGD patient (patient 1). This organism was subsequently isolated from the same patient three more times throughout 2005. A similar Gram-negative rod was isolated from two other CGD patients in December 2005 (patient 2) and in January 2006 (patient 3). Phenotypic and genotypic analyses are consistent with this being a previously undescribed bacterium in the group of acetic acid bacteria. Whole genome sequencing of the first isolate from patient 1 was performed and the sequence was deposited in the GenBank/EMBL/DDBJ databases as accession number CP000394. In this paper, we give a detailed description of the characteristics of these isolates and propose that they represent a new genus and species, Granulibacter bethesdensis gen. nov., sp. nov.
Lymph nodes from patient 1 were ground and inoculated onto various media. On initial isolation from patient 1, colonies were visible after 46 days of incubation on buffered charcoal yeast extract (BCYE) agar, Sabouraud dextrose agar, inhibitory mould agar and Middlebrook 7H11 agar, in either ambient air at 30 °C or 7 % CO2 at 35 °C. The isolate from patient 2 grew after 8 days in a commercial broth used for the isolation of mycobacteria (BD Bactec MGIT 960; Becton Dickinson). The isolate from patient 3 grew after 5 days on BCYE agar. Details of patient history and data on histology and pathogenicity in mice are discussed elsewhere (Greenberg et al., 2006
).
For the characterization of the novel organism, we took a polyphasic taxonomic approach, using phenotypic data in the form of biochemical tests and a multilocus DNA sequence analysis for phylogenetic reconstruction. For the multilocus approach, we focused on (i) the 16S rRNA gene, (ii) the internal transcribed spacer (ITS) region and (3) the RecA protein. The first two loci have been used extensively in the phylogenetic analysis of the Acetobacteraceae (Tanasupawat et al., 2004
; Ruiz et al., 2000
; Lisdiyanti et al., 2000
, 2002
), whereas the RecA protein has been described as a model molecule for systematic studies between related species of the Alphaproteobacteria, generally producing results congruent with those obtained from 16S rRNA gene data (Eisen, 1995
).
Phenotypic identification was initially attempted with commercial biochemical kits and supplementary phenotypic tests routinely used in clinical microbiology. Kits included API 20 NE (bioMérieux) and RapID NH (Remel), neither of which yielded an identification. Supplementary phenotypic characterization included tests for oxidase, catalase, oxidativefermentative medium with either glucose, lactose, mannitol, sucrose, maltose or xylose (OF medium King; Remel), lysine- and ornithine decarboxylases (Remel), arginine dihydrolase (Remel), urease (Rapid Urea Slant; Hardy Diagnostics) and motility (Motility Test Medium; Hardy Diagnostics). Growth on methanol as a sole carbon source was performed on medium 569 (Sievers & Swings, 2005
). Additional tests used for the acetic acid bacteria (Table 1
) as well as morphological and physiological characterizations were carried out as described by Asai et al. (1964)
and Shimwell et al. (1960)
.
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Cells of the novel organism were Gram-negative, coccobacillus to rod-shaped and non-motile. The bacterium was obligately aerobic, catalase-positive and oxidase-negative. Lysine- and ornithine decarboxylases and arginine dihydrolase were all negative. Urease was positive for the isolates from patients 1 and 2, but was weak or negative for the isolate from patient 3; there was weak acid production from glucose, but no acid production from lactose, mannitol, sucrose, maltose or xylose. The bacterium grew on glutamate and mannitol agars. It oxidized lactate and acetate to carbon dioxide and water, but the activity of the latter was weak. For tests for ketogenic activity on glycerol (dihydroxyacetone production), 1 g glucose l1 was added to the glycerol medium because the organism failed to grow on the medium described by Shimwell et al. (1960)
. The bacterium did not produce dihydroxyacetone from glycerol. The organism grew on methanol as a sole carbon source. It generated acetic acid poorly on ethanol-CaCO3 agar (with 2 % CaCO3) (Asai et al., 1964
). Acetic acid production was more evident on modified ethanol-CaCO3 agar plates containing lower concentrations of CaCO3. The results of these and additional biochemical tests are summarized in Table 1
.
Cellular fatty acid analysis was performed as described by Weyant et al. (1996)
. The major fatty acids were a straight-chain unsaturated acid (C18 : 1
7c) and C16 : 0, which accounted for 50 and 17 % of the total cellular fatty acids, respectively. Other fatty acids identified were C19 : 0cyc1112 (10 %) and smaller amounts of 2-OH C14 : 0, sum of 3-OH C14 : 0 and/or i-C16 : 1I, 3-OH C16 : 0, C17 : 0, C17 : 1
6c, C18 : 0, 2-OH C18 : 1, 2-OH C16 : 0, C16 : 1
7c and 3-OH C18 : 0.
DNADNA relatedness was determined by using the hybridization method described by Brenner et al. (1982)
. Purified DNA of the first isolate from patient 1 (type strain) and the isolates from patient 2 and patient 3 were prepared from lysed protoplasts based on a protocol described by Loeffelholz & Scholl (1989)
. In brief, bacteria grown in SOC broth were incubated for 2 h at 37 °C with 2 mg lysozyme ml1 in 0.05 M TE buffer (pH 8.0), followed by overnight incubation at 56 °C with proteinase K (50 µg ml1), SDS (0.5 %) and NaCl (0.1 M). Nucleic acids were purified by the phenol/chloroform/isoamyl alcohol (25 : 24 : 1, by vol.) method and treated with RNase, followed by three washes with chloroform/isoamyl alcohol (24 : 1, v/v) and sodium acetate precipitation. Subsequent isolates from patient 1 were undistinguishable from the first isolate by PFGE and repetitive sequence-based PCR (data not shown) and therefore were not assayed for DNADNA relatedness. DNA was labelled with [32P]dCTP by using a nick translation kit (Gibco). All reactions were performed in duplicate at 63 °C. The relative binding ratio (RBR) [(percentage of heterologous DNA bound to hydroxyapatite/percentage of homologous DNA bound to hydroxyapatite)x100] was calculated by using methods described by Brenner et al. (1983)
. Labelled DNA from the isolate from patient 1 showed 97 and 93 % DNADNA relatedness to the isolates from patients 2 and 3, respectively. When the DNA from the isolate from patient 3 was labelled, the DNADNA relatedness values were 90 and 92 % to the isolates of patients 1 and 2, respectively. By using the accepted interpretive criteria (an RBR greater than 70 %) (Brenner et al., 1983
; Wayne et al., 1987
), the DNADNA hybridization results confirmed that the three isolates represent a single species.
DNA was isolated using a NucliSens kit (bioMérieux). The 16S rRNA genes of the isolates from the three patients were PCR-amplified and sequenced using a MicroSeq Full Gene 16S rRNA Bacterial Isolation sequencing kit (Applied Biosystems), according to the manufacturer's protocol. Sequences were analysed using a 3100 Genetic Analyzer (Applied Biosystems). The Lasergene program (version 5.51; DNASTAR) was used for sequence assembly and alignment. The 16S rRNA gene sequences of the patients' isolates were compared with 16S rRNA gene sequences available in the GenBank/EMBL/DDBJ databases. The isolates from the three patients had identical 16S rRNA gene sequences.
Preliminary whole genome sequencing for Granulibacter bethesdensis (patient 1, first isolate) was performed using methods that have been used for several other bacteria (DelVecchio et al., 2002
; Kapatral et al., 2002
; Ivanova et al., 2003
; D. E. Greenberg and others, unpublished results). The 16S rRNA gene, ITS region and the RecA protein-encoding gene were collected by BLAST searching of the preliminary genome assembly. Nucleotide and deduced amino acid sequences for targeted genes were analysed initially with MacVector version 6.0/7.0 software package (Oxford Molecular). DNA sequences were first aligned with the CLUSTAL W program in the lasergene software package (DNASTAR). Alignments for the 16S rRNA gene, ITS region and RecA sequences were performed following standard procedures provided by the manufacturer (DNASTAR). The alignments were transferred into the MacClade program (Maddison & Maddison, 2003
) for removal of insertions/deletions (indels), sequence errors, equalizing sequence lengths and manual correction of the alignments. MacClade output files were opened in PAUP (Swofford, 2002
) with an include all line command. For the 16S rRNA gene, ITS region and RecA protein, maximum-likelihood neighbour-joining trees were created with a paraphyletic outgroup. The robustness of clade designations was tested with a full heuristic search and 1000 bootstrap replicates. The nucleotide sequence for the ITS region of Rhodospirillium rubrum was obtained from the Rhodospirillium rubrum genome project of the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/).
During genome sequencing, three homologous 16S23S rRNA gene loci were discovered. The 16S rRNA gene was 1482 bases in length and was identical at all three loci. BLAST searches indicated that the 16S rRNA gene sequence was most similar to sequences of other organisms in the family Acetobacteraceae. Because 16S rRNA gene sequences are of varying lengths in the database, CLUSTAL W alignments were used to identify a conserved, common, internal 1381 bp region, among multiple representatives of the Acetobacteraceae. This region spanned positions 331413 of the 16S rRNA gene of our bacterium. Eighteen 16S rRNA gene sequences of representative taxa or type strains within and related to the family Acetobacteraceae were collected from NCBI and the resulting phylogenetic tree is shown in Fig. 1
. Multiple iterations of 16S rRNA gene analyses were performed with many different species and strains of Acetobacteraceae with no strains similar to our bacterium detected (data not shown). Phylogenetic groupings of representatives of the genera Acetobacter, Gluconobacter, Saccharibacter, Swaminathania, Neoasaia, Gluconacetobacter, Acidomonas, Asaia and Kozakia, as shown in Fig. 1
are similar to what has previously been published (Jojima et al., 2004
; Loganathan & Nair, 2004
; Tanasupawat et al., 2004
; Yukphan et al., 2004a
, b
, 2005
) (Fig. 1
). The 16S rRNA gene sequence of strain CGDNIH1T grouped within the family Acetobacteraceae, whereas the branch length and positioning indicated that it warrants separate genus-level status (Fig. 1
). Percentage similarity values for the novel bacterium compared with representative members of the Acetobacteraceae ranged from 95.4 % with Gluconacetobacter liquefaciens to 86.0 % with Stella humosa (Table 2
).
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Acetic acid bacteria have been isolated from fruits, fermented foods, plants, soil and water, and are important in the food and biotechnology industry (Seearunruangchai et al., 2004
; Sokollek et al., 1998
). Based on 16S rRNA gene sequence analysis, these bacteria are associated with a group of acidophilic bacteria in the Alphaproteobacteria (Sievers et al., 1995
). The novel organism shows unique phenotypic characteristics compared with isolates belonging to the nine described genera of acetic acid bacteria, and therefore clearly represents a new taxon. Like Acidomonas methanolica, the novel bacterium is a facultative methylotroph that is able to use methanol as a sole carbon source. However, it is distinguished from Acidomonas methanolica in that it generates acetic acid poorly on ethanol-CaCO3 agar (with 2 % CaCO3), oxidizes lactate and grows on glutamate and mannitol agar, and forms colonies that are yellow-pigmented. Whereas the optimum temperature for growth of most acetic acid bacteria is
30 °C, the novel organism prefers higher temperatures (3537 °C). The fatty acid profile was roughly in agreement with those reported for other genera in the acetic acid bacteria, with the predominant fatty acid being C18 : 1
7c (Franke et al., 1999
); however, the novel bacterium contained relatively high amounts of the cyclopropane fatty acid C19 : 0cyc1112.
Multilocus sequence analysis is a widely accepted method for identifying and analysing novel genera and species or differentiating strains or isolates (Garcia-Martinez et al., 1999
; Owen, 2004
; Ludwig et al., 1998
; Zeigler, 2003
). Because of the distinctiveness of the novel organism, we undertook a multilocus sequence analysis in an effort to definitively determine the phylogenetic position of this organism. Our analyses of the 16S, ITS and RecA sequences broadly support previously published findings for members of the Acetobacteraceae (Tanasupawat et al., 2004
; Yamada et al., 2000
; Cleenwerck et al., 2002
), while establishing a separate lineage for our organism. Our results confirm that the isolate represents a member of the Acetobacteraceae, yet is distinct enough to warrant separate genus-level designation. The name Granulibacter bethesdensis gen. nov., sp. nov. is proposed.
Description of Granulibacter gen. nov.
Granulibacter (Gra.nu.li.bac'ter. L. neut. n. granulum grain; N.L. masc. n. bacter from Gr. n. baktron rod; N.L. masc. n. Granulibacter a rod that causes granules or granuloma formation).
Cells are Gram-negative, non-motile and coccobacillus to rod-shaped. Strictly aerobic. Catalase-positive. Oxidase-negative. Urease variable. Produce a yellow pigment. Optimum temperature for growth is 3537 °C. Optimum pH for growth is 5.06.5. Oxidize lactate and acetate to carbon dioxide and water, but the activity of the latter is weak. Produce little acetic acid from ethanol. Can use methanol as a sole carbon source. Prefer high glucose concentration for growth [e.g. 5 % (w/v) glucose]. Grow on glutamate agar and on mannitol agar. Ammoniacal nitrogen is assimilated on glucose medium. Do not produce dihydroxyacetone from glycerol. Acid is produced from glucose and ethanol and variably from glycerol (weak or negative reactions), but not from mannitol, sorbitol, dulcitol, lactose, sucrose, maltose or xylose. DNA base composition is 59.1 mol% G+C. The type species is Granulibacter bethesdensis.
Description of Granulibacter bethesdensis sp. nov.
Granulibacter bethesdensis (be.thes.den'sis. N.L. masc. adj. bethesdensis pertaining to Bethesda, MD, USA, where the type strain was isolated).
Characteristics are the same as those described for the genus. The type strain is strain CGDNIH1T (=ATCC BAA-1260T=DSM 17861T), which was isolated from lymph node cultures from a chronic granulomatous disease patient in Bethesda, MD, USA, in 2003.
| ACKNOWLEDGEMENTS |
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