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Division of Biology and Ocean Sciences, Inha University, Yonghyun-Dong, Incheon 402-751, Republic of Korea
Correspondence
Jang-Cheon Cho
chojc{at}inha.ac.kr
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; Haukka et al., 2005; Hugenholtz et al., 1998; O'Farrell & Janssen, 1999), only a few members of the phylum have yet been cultivated (Chin et al., 2001; Derrien et al., 2004; Hedlund et al., 1997; Hugenholtz et al., 1998; Sangwan et al., 2004; Schlesner, 1987; Ward-Rainey et al., 1995). The phylum ‘Verrucomicrobia’ has been divided historically into five subdivisions, V1 to V5, based on 16S rRNA gene sequences (Hugenholtz et al., 1998). In the second edition of Bergey's Manual of Systematic Bacteriology (Garrity et al., 2003), however, three subdivisions are included at the rank of family: the families Verrucomicrobiaceae (subdivision 1), ‘Xiphinematobacteriaceae’ (subdivision 2) and ‘Opitutaceae’ (subdivision 4). Subdivision 1 includes the freshwater species Verrucomicrobium spinosum (Schlesner, 1987), four freshwater species of the genus Prosthecobacter (Hedlund et al., 1996, 1997) and the human-intestinal species Akkermansia muciniphila (Derrien et al., 2004). Subdivision 2 contains only one cultured species, the recently identified ‘Chthoniobacter flavus’ (Sangwan et al., 2004). There are three identified species in subdivision 4, the soil-borne species Opitutus terrae (Chin et al., 1999, 2001; Janssen et al., 1997), Alterococcus agarolyticus (Shieh & Jean, 1998), isolated from a hot spring and originally misclassified within the class Gammaproteobacteria, and ‘Fucophilus fucoidanolyticus’, isolated from a sea cucumber (Sakai et al., 2003). Here we report the characterization of a verrucomicrobial isolate cultured from the digestive tract of a marine clamworm. Taxonomic analyses indicated that this marine clamworm-associated isolate is distantly related to members of subdivision 4 of the phylum ‘Verrucomicrobia’ and represents a novel genus and species within subdivision 4. In addition, to clarify the taxonomic outline of subdivision 4 of the phylum ‘Verrucomicrobia’, we formally propose Opitutae classis nov., which is composed of two novel orders, Puniceicoccales ord. nov., containing Puniceicoccaceae fam. nov., and Opitutales ord. nov., containing Opitutaceae fam. nov.
Benthic marine worms of the species Periserrula leucophryna (family Nereididae), a polychaete species endemic to the west coast of Korea, were collected in July 2005 from a depth of 1–2 m from tidal flat sediments on Donggum island (37° 35' 34.1'' N 126° 31' 7.5'' E). The marine worms were washed three times with sterile seawater and dissected under an Olympus SZH10 stereoscopic microscope. Entire invertebrate homogenates, digestive tract tissue homogenates and soil-like aggregates from within the digestive tract were used for isolating marine invertebrate-associated micro-organisms. One hundred microlitre aliquots of tissue homogenate were spread onto marine 2216 agar (MA; Difco) and the agar plates were incubated aerobically at 20 °C for 5, 14 or 30 days. A strain, designated strain IMCC1545T, was initially isolated from a digestive tract tissue homogenate after incubation for 14 days. The strain was purified as single colonies on MA at 30 °C and was stored as 10 % (v/v) glycerol suspensions at –80 °C. Unless otherwise indicated, cultures of the strain were grown routinely on MA at 30 °C.
Phenotypic characterizations were performed as described in previous studies (Cho & Giovannoni, 2003; Smibert & Krieg, 1994) using MA as the basal medium at 30 °C, unless otherwise noted. Cell morphology was examined by scanning electron microscopy (JSM 5410LV; JEOL), energy-filtering transmission electron microscopy (LIBLA120; Carl Zeiss) and phase-contrast microscopy (Nikon 80i; Nikon). Anaerobic growth was tested on MA at 30 °C using both the MGC anaerobic system and AnaeroPACK.Anaero (Mitsubishi Gas Chemical Company). Biochemical tests were carried out on API 20NE and API ZYM (bioMérieux) according to the manufacturer's instructions with artificial seawater (l–1: 25.0 g NaCl, 1.0 g MgCl2.6H2O, 5.0 g MgSO4.7H2O, 0.7 g KCl, 0.15 g CaCl2.2H2O, 0.5 g NH4Cl, 0.1 g KBr, 0.27 g KH2PO4, 0.04 g SrCl2.6H2O, 0.025 g H3BO3). Pigments of strain IMCC1545T were extracted with acetone/methanol (1 : 1, v/v) and absorption spectra were determined using a scanning UV/visible spectrophotometer (Optizen 2120UV; Mechasis). The ability of the strain to oxidize 95 different carbon sources was determined using Biolog GN2 microplates with artificial seawater. The following antibiotics were tested: ampicillin (10 µg), chloramphenicol (25 µg), erythromycin (15 µg), gentamicin (10 µg), kanamycin (30 µg), penicillin G (10 µg), rifampicin (50 µg), streptomycin (10 µg), tetracycline (30 µg) and vancomycin (30 µg).
Cells of strain IMCC1545T are cocci, 0.6–1.0 µm in diameter (Fig. 1). No flagella were found. Carotenoid pigments with absorbance spectrum peaks at 320 and 480 nm were found; the latter peak was minutely separated into three peaks at 450, 480 and 504 nm. Anaerobic cultures grew much slower than aerobic cultures. In the API 20NE test, tests for nitrate reduction, indole production, glucose fermentation, arginine dihydrolase, urease, aesculin hydrolysis, gelatinase and PNPG (
-galactosidase) were negative. In the API ZYM test, positive reactions were observed for alkaline phosphatase, esterase (C4), esterase lipase (C8), acid phosphatase and naphthol-AS-BI-phosphohydrolase and negative reactions were observed for lipase (C14), leucine, valine and cystine arylamidases, trypsin, 
-chymotrypsin, -galactosidase, -galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase. In tests with Biolog GN2 microplates, the strain utilized the following carbon compounds oxidatively: dextrin, D-arabitol, L-arabinose (weakly), D-cellobiose, D-fructose, D-galactose, gentiobiose, -D-glucose, -D-lactose, maltose, D-mannitol, D-mannose, methyl -D-glucoside, D-psicose (weakly), L-rhamnose, D-sorbitol, sucrose, D-trehalose, turanose, pyruvic acid methyl ester (weakly), succinic acid monomethyl ester, D-galactonic acid lactone, -hydroxybutyric acid, -ketobutyric acid (weakly), -ketoglutaric acid, -ketovaleric acid (weakly), DL-lactic acid, succinic acid, succinamic acid (weakly), L-pyroglutamic acid, DL-carnitine (weak), 2,3-butanediol, glycerol, DL--glycerol phosphate, -D-glucose 1-phosphate and D-glucose 6-phosphate. Strain IMCC1545T did not utilize the remaining compounds of the GN2 microplate. The strain was resistant to ampicillin, chloramphenicol, gentamicin, kanamycin, penicillin G, rifampicin, streptomycin and vancomycin and susceptible to erythromycin and tetracycline.
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). Respiratory quinones were analysed using reverse-phase HPLC by the Korea Culture Center of Micro-organisms (KCCM). Cellular fatty acid methyl esters were prepared from a culture grown on MA at 30 °C for 5 days and analysed according to the instructions of the Microbial Identification System (MIDI) by KCCM. The DNA G+C content of strain IMCC1545T was 52.1±0.5 mol%. The only respiratory quinone detected was menaquinone-7. The major fatty acids in strain IMCC1545T were anteiso-C15 : 0 (30.9 %), C18 : 0 (24.7 %), C16 : 0 (7.9 %) and C17 : 0 (7.0 %). Characteristics that differentiate strain IMCC1545T from other members of subdivision 4 of the phylum ‘Verrucomicrobia’ are listed in Table 1.
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) and used for phylogenetic and comparative sequence analyses. Preliminary BLASTN network searches in GenBank showed that the strain belongs to the phylum ‘Verrucomicrobia’. According to comparative 16S rRNA gene sequence analyses based on the BLASTN searches, the closest named species to strain IMCC1545T were ‘Fucophilus fucoidanolyticus’ (86.5 % sequence similarity to the proposed type strain SI-1234), Alterococcus agarolyticus (81.8 % similarity to strain ADT3T) and Opitutus terrae (80.3 % similarity to strain PB90-1T), and thus the strain was initially considered a novel member of the phylum ‘Verrucomicrobia’. To clarify the phylogenetic position of strain IMCC1545T, its 16S rRNA gene sequence was aligned carefully using the ARB package (Ludwig et al., 2004) and only 1036 unambiguously aligned nucleotide positions were used for phylogenetic analyses in the ARB package and PAUP* version 4.0 beta 10 (Swofford, 2002). Neighbour-joining, maximum-parsimony and maximum-likelihood phylogenetic trees were generated as described previously (Cho et al., 2004).
In all the phylogenetic trees generated, strain IMCC1545T formed a tight clade together with the uncultured lake bacterium K2-S-20 within subdivision 4 of the ‘Verrucomicrobia’ (Fig. 2). This clade was strongly supported by high bootstrap values (100 % in both neighbour-joining and maximum-parsimony trees) and clearly separated from the nearest clade containing ‘Fucophilus fucoidanolyticus’, suggesting that strain IMCC1545T should be placed in a novel genus and species. A large clade containing both ‘Fucophilus fucoidanolyticus’ and strain IMCC1545T, in spite of low bootstrap support, was clearly separated from a clade containing Opitutus terrae. Members of the large clade containing strain IMCC1545T shared only 78.4–82.1 % 16S rRNA gene sequence similarity with members of the adjacent clade containing Opitutus terrae, suggesting that these two clades should be ranked as separate higher taxa, such as novel families or orders. Based on sequence information available from GenBank, the clade containing strain IMCC1545T consists mainly of uncultured marine and aquatic bacteria and the clade containing Opitutus terrae consists largely of soil bacteria, indicating a habitat-specific distribution of members of the two clades.
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). The G+C contents of strain IMCC1545T and ‘Fucophilus fucoidanolyticus’ SI-1234 were 13.7–21.8 mol% lower than those of Alterococcus agarolyticus and Opitutus terrae, showing a distinct genetic difference between the two clades. Recently, the class ‘Spartobacteria’ and the order ‘Chthoniobacterales’ were proposed as new names equivalent to subdivision 2 of the phylum ‘Verrucomicrobia’ (Sangwan et al., 2004). Similar to the above proposal, we formally propose the name Opitutae classis nov. for subdivision 4 of the phylum ‘Verrucomicrobia’, which contains Opitutales ord. nov. and Puniceicoccales ord. nov. We also propose the names Puniceicoccaceae fam. nov. and Opitutaceae fam. nov. for the clades containing strain IMCC1545T and the genus Opitutus, respectively, together with a novel genus and species, Puniceicoccus vermicola gen. nov., sp. nov., for strain IMCC1545T.
Description of Opitutae classis nov.
Opitutae (O.pi.tu'tae. N.L. fem. pl. n. Opitutales type order of the class; -ae ending to denote a class; N.L. fem. pl. n. Opitutae the class of the order Opitutales).
Equivalent to subdivision 4 (Hugenholtz et al., 1998) of the phylum ‘Verrucomicrobia’ and is defined by phylogenetic analyses based on 16S rRNA gene sequences obtained from four cultured representatives and a wide range of uncultured bacteria retrieved mainly from marine and soil habitats. Gram-negative. The class comprises the order Opitutales and the order Puniceicoccales. The type order is the order Opitutales.
Description of Opitutales ord. nov.
Opitutales (O.pi.tu.ta'les. N.L. masc. n. Opitutus type genus of the order; -ales ending to denote an order; N.L. fem. pl. n. Opitutales the order of the genus Opitutus).
Encompasses Gram-negative bacteria retrieved mainly from soil environments, within the class Opitutae of the phylum ‘Verrucomicrobia’. The order contains the family Opitutaceae. Delineation of the order is determined primarily by phylogenetic information from 16S rRNA gene sequences. The type genus is the genus Opitutus (Chin et al., 2001).
Description of Puniceicoccales ord. nov.
Puniceicoccales (Pu.ni.cei.coc.ca'les. N.L. masc. n. Puniceicoccus type genus of the order; -ales ending to denote an order; N.L. fem. pl. n. Puniceicoccales the order of the genus Puniceicoccus).
Encompasses Gram-negative bacteria retrieved mainly from marine environments, within the class Opitutae. The order contains the family Puniceicoccaceae. Delineation of the order is determined primarily by phylogenetic information from 16S rRNA gene sequences. The type genus is the genus Puniceicoccus.
Description of Opitutaceae fam. nov.
Opitutaceae (O.pi.tu.ta'ce.ae. N.L. masc. n. Opitutus type genus of the family; -aceae ending to denote a family; N.L. fem. pl. n. Opitutaceae the family of the genus Opitutus).
Encompasses Gram-negative bacteria retrieved mainly from soil and terrestrial environments, including a hot spring and wood, within the order Opitutales. Currently, the family comprises the genera Opitutus and Alterococcus, together with several uncultured bacteria retrieved mainly from soil environments. Delineation of the family is determined primarily by phylogenetic information from 16S rRNA gene sequences. Gram-negative, motile, facultatively or obligately anaerobic cocci. The DNA G+C content of members of the family is 65–74 mol%. The type genus is the genus Opitutus (Chin et al., 2001).
Description of Puniceicoccaceae fam. nov.
Puniceicoccaceae (Pu.ni.cei.coc.ca'ce.ae. N.L. masc. n. Puniceicoccus type genus of the family; -aceae ending to denote a family; N.L. fem. pl. n. Puniceicoccaceae the family of the genus Puniceicoccus).
Encompasses Gram-negative bacteria retrieved mainly from marine and aquatic environments, within the order Puniceicoccales. Currently, the family comprises the genus Puniceicoccus and ‘Fucophilus fucoidanolyticus’, together with several uncultured marine and lake bacteria. Delineation of the family is determined primarily by phylogenetic information from 16S rRNA gene sequences. The detailed description is the same as for the genus Puniceicoccus. The type genus is the genus Puniceicoccus.
Description of Puniceicoccus gen. nov.
Puniceicoccus (Pu.ni.cei.coc'cus. L. adj. puniceus pinkish red; N.L. masc. n. coccus from Gr. masc. n. kokkos a berry; N.L. masc. n. Puniceicoccus a pinkish-red-coloured coccus).
Cells are Gram-negative, non-motile, facultatively anaerobic cocci (oval-shaped, 0.6–1.0 µm in diameter). Carotenoid pigments are found. Require NaCl for growth. The predominant fatty acids are anteiso-C15 : 0 and C18 : 0. The only respiratory quinone detected is menaquinone-7. The DNA G+C content is 52.1±0.5 mol%. The type and only species of the genus is Puniceicoccus vermicola.
Description of Puniceicoccus vermicola sp. nov.
Puniceicoccus vermicola (ver.mi'co.la. L. n. vermis worm; L. suff. -cola from L. n. incola inhabitant; N.L. n. vermicola inhabitant of worms).
In addition to the characteristics reported for the genus, the following are added. Colonies on MA are uniformly circular, smooth, convex, opaque, pale-reddish coloured and 0.3–0.5 mm in diameter after 5 days of incubation. Colonies are up to 3 mm in diameter after 3 weeks of incubation. Growth occurs at 8–37 °C, optimally at 25–30 °C, but not at 4 or 42 °C. Growth occurs at pH 5–12 and 1.0–7.5 % NaCl, occurring optimally at pH 9.0 and 3.0–3.5 % NaCl. Oxidase and catalase are negative. Other phenotypic characteristics, including biochemical properties, carbon source utilization, enzyme activities and susceptibility to antibiotics, are given in the text. The fatty acids detected in the type strain are anteiso-C15 : 0 (30.9 %), C18 : 0 (24.7 %), C16 : 0 (7.9 %), C17 : 0 (7.0 %), iso-C14 : 0 (5.3 %), C14 : 0 (4.9 %), anteiso-C17 : 0 (3.6 %), C18 : 0 3-OH (2.5 %) and C12 : 0 3-OH (2.1 %).
The type strain, IMCC1545T (=KCCM 42343T=NBRC 101964T), was isolated from the digestive tract of a sea polychaete (Periserrula leucophryna) inhabiting a tidal flat of Donggum island, Korea.
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ACKNOWLEDGEMENTS |
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