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1 Center for General Education, Leader University, No. 188, Sec. 5, An-Chung Rd, Tainan, Taiwan
2 Institute of Oceanography, National Taiwan University, PO Box 23-13, Taipei, Taiwan
Correspondence
Wung Yang Shieh
winyang{at}ntu.edu.tw
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ABSTRACT |
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8c (12.8 %), C17 : 0 (11.1 %), C15 : 0 iso 2-OH/C16 : 17c (8.6 %) and C13 : 0 (7.3 %). The DNA G+C content was 41.0 mol%. Phylogenetic, phenotypic and chemotaxonomic data accumulated in this study revealed that the isolate could be classified in a novel species of the genus Thalassomonas in the family Colwelliaceae. The name Thalassomonas agarivorans sp. nov. is proposed for the novel species, with TMA1T (=BCRC 17492T=JCM 13379T) as the type strain.
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); taxonomic affiliation of Oceanimonas and Oceanisphaera at the family level remained undetermined.
Agar, a complex polysaccharide extracted from marine red algae, is widely employed as a gelling agent for microbiological culture media. This refractory material is attacked by relatively few bacterial species (Holt et al., 1994). Agarolytic bacteria are ubiquitous in coastal and estuarine regions; however, they are not exclusively autochthonous in the marine environment, since some reports have shown that they also occur in freshwater, sewage and soil (Agbo & Moss, 1979; van der Meulen et al., 1974; von Hofsten & Malmqvist, 1975). Several marine agarolytic strains of Vibrio-like species have been demonstrated to be capable of fixing N2 for anaerobic growth using agar as the sole source of carbon and energy (Shieh et al., 1988). A Vibrio species, Vibrio agarivorans, is also reported to be capable of decomposing agar in addition to these unnamed, Vibrio-like agarolytic strains (Macián et al., 2001b). Alterococcus agarolyticus, the only thermophilic agarolytic species, is a marine, facultatively anaerobic, fermentative, Gram-negative coccus growing between 38 and 58 °C with optimum growth at about 48 °C (Shieh & Jean, 1998). No other agarolytic bacteria have been reported to grow at temperatures of 45 °C or higher. Only a handful of species belonging to the Alteromonas-like Gammaproteobacteria such as Pseudoalteromonas atlantica (Akagawa-Matsushita et al., 1992; Gauthier et al., 1995), Pseudoalteromonas agarivorans (Romanenko et al., 2003a), Glaciecola mesophila (Romanenko et al., 2003b) and Shewanella olleyana (Skerratt et al., 2002) are agarolytic or weakly agarolytic. Recently, strain JAMB-A33, an agarolytic bacterium which produces a novel 
-agarase, was isolated from the sediment off Noma Point, Japan (Ohta et al., 2005). Phylogenetic analysis of 16S rRNA gene sequences suggested that this isolate might represent a novel species of Thalassomonas in the Alteromonas-like Gammaproteobacteria. However, classification of this isolate on the basis of phenotypic and chemotaxonomic features was not reported (Ohta et al., 2005). Evidence is presented here that an agarolytic bacterium isolated in this laboratory can be classified in a novel species in the genus Thalassomonas.
An-Ping Harbour of Tainan is a small harbour located on the south-west coast of Taiwan. A seawater sample collected from the shallow water region of this harbour was decimally diluted with sterile NaCl/Tris buffer (30 g NaCl and 0.24 g Tris in 1 l deionized water, pH 8.0). Aliquots (0.1 ml) of the decimal dilutions (102–104 times) were spread on PY (Polypepton/yeast extract) plate medium (Shieh et al., 2000). The plates were incubated at 25 °C in the dark for 7 days under aerobic conditions. Strain TMA1T, appearing as an agarolytic off-white colony, was isolated from one of the plates and subsequently purified by successive streaking on PY plates. Its maintenance in our laboratory was performed repeatedly at an interval of 2–3 months by inoculating early stationary phase cultures grown in PY broth into 7/10-strength seawater at a ratio of 2 : 50 (v/v). Maintenance cultures were kept at 20 °C. The isolate has also been deposited in both JCM and BCRC by lyophilization.
Strain TMA1T was cultivated aerobically in PY broth at 25 °C in the dark for 3 days. Cells were harvested by centrifugation. Total genomic DNA was extracted and purified from the cells by using a Puregene DNA isolation kit (Gentra Systems) in accordance with the manufacturer's instructions. Hydration solution of the purified DNA sample was prepared at concentrations of 500 µg ml–1. The DNA hydration solution was used for PCR amplification (Jean et al., 2006).
Sequencing of the 16S rRNA gene sample, alignment and comparison of the resulting sequence and reference sequences available in the GenBank database, calculation of distance matrices for the aligned sequences and reconstruction of a phylogenetic tree by the neighbour-joining method were carried out as described by Shieh et al. (2004). Phylogenetic trees were also reconstructed by using maximum-parsimony (Fitch, 1971) and maximum-likelihood (Felsenstein, 1981) methods. The accession numbers for the sequences used to reconstruct the phylogenetic tree are shown in Fig. 1. Bootstrap confidence values (Felsenstein, 1985) were obtained with 1000 resamplings with an option of stepwise addition.
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). This work was performed at the Bioresources Center for Research and Collection (BCRC), Food Industry Research and Development Institute, Taiwan. DNA G+C content was determined by HPLC analysis (Shieh & Liu, 1996), which was also performed at BCRC. DNA–DNA relatedness between strains TMA1T and Thalassomonas loyana CBMAI 722T was determined as described by Shieh et al. (2003a).
Growth and other phenotypic characteristics of strain TMA1T were examined by the methods of Shieh et al. (2000) with modifications and additional tests as described below. Growth at different temperatures was determined in PY broth and recorded daily for up to 5 days at 20, 25, 30, 35, 37 and 40 °C and for 20 days at 4, 10, 13 and 15 °C, unless significant growth had been observed. Growth at various NaCl levels was determined in PY broth containing 0, 0.5, 1, 2, 3, 4, 5, 6, 7 or 8 % NaCl. Anaerobic growth in PY, PYG (Polypepton/yeast extract/glucose) and PYN (Polypepton/yeast extract/nitrate) broth media under argon gas was examined as described by Shieh et al. (2004). Utilization of various carbohydrates and other compounds as sole carbon and energy sources for growth was determined in CM (carbohydrate/mineral) media (Shieh et al., 2004) or modifications containing 0.2 % of any one of the test organic acids or amino acids used in place of the carbohydrates. The test compounds included glucose, D-arabinose, L-arabinose, cellobiose, fructose, galactose, lactose, maltose, mannose, melibiose, sucrose, trehalose, xylose, glycerol, dulcitol, inositol, mannitol, acetate, citrate, fumarate, 
-hydroxybutyrate, malonate, tartrate, L-alanine, arginine, aspartate, gluconate, glutamine, glutamate, leucine, lysine, tryptophan and L-aconitate. H2S production from thiosulphate was tested as described by Shieh et al. (2004). Urease, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase and hydrolysis of aesculin, alginate and lecithin were tested by methods similar to those of Smibert & Krieg (1994): the urease test was carried out with Christensen urea agar (Smibert & Krieg, 1994) containing 25 g NaCl l–1 instead of the original 5 g l–1. A modified PY plate medium containing egg-yolk emulsion (100 ml l–1) was used to test the hydrolysis of lecithin. Modified plate media containing aesculin (1 g l–1) and alginate (10 g l–1), respectively, were used to test hydrolysis of these substrates. Tests for arginine dihydrolase, lysine decarboxylase and ornithine decarboxylase were performed in broth media containing Bacto decarboxylase base Moeller (Difco), NaCl (25 g l–1), MgCl2.6H2O (2 g l–1) and the appropriate L-amino acid (10 g l–1). Other constitutive enzyme activities were detected by using the API ZYM system (bioMérieux Vitek). Cell suspensions used for these tests were prepared by suspending the cells in a mineral medium containing 0.54 g NH4Cl, 30 g NaCl, 3 g MgCl2.6H2O, 2 g K2SO4, 0.2 g K2HPO4, 0.01 g CaCl2, 0.006 g FeCl3.6H2O, 0.005 g Na2MoO4.7H2O, 0.004 g CuCl2.2H2O and 6 g Tris base dissolved in 1000 ml deionized water and adjusted to pH 8.0. Antibiotic susceptibility tests were performed by disc-diffusion methods as described in our previous reports (Shieh et al., 2003a, b). All test cultures were incubated aerobically at 25 °C in the dark for 7 days, unless stated otherwise.
An almost-complete 16S rRNA gene sequence of strain TMA1T (1465 bp) was determined. The sequence was aligned and compared with all bacterial sequences available in the GenBank database. Phylogenetic analysis of the 16S rRNA gene sequences revealed that strain TMA1T was a member of the Alteromonas-like bacteria in the Gammaproteobacteria. The strain showed highest sequence similarities to strain JAMB-A33 (98.2 %), T. loyana CBMAI 722T (97.0 %), Thalassomonas ganghwensis JC2041T (95.2 %) and Thalassomonas viridans CECT 5083T (94.7 %); strain JAMB-A33 has not been classified on the basis of phenotypic and chemotaxonomic features. Besides members of Thalassomonas, species of Colwellia were the closest relatives of strain TMA1T (93.2–93.8 % sequence similarity). No other known bacteria shared more than 91 % sequence similarity with strain TMA1T. The phylogenetic tree derived from neighbour-joining analysis indicated that strains TMA1T and JAMB-A33 formed a separate taxon in the genus Thalassomonas, which was supported by a bootstrap value of 100 % (Fig. 1
). Similar results were obtained from maximum-likelihood and maximum-parsimony algorithms (not shown).
Strain TMA1T contained C16 : 0 as the most abundant fatty acid (17.5 %). Other major fatty acids present at levels greater than 5 % included C17 : 18c (12.8 %), C17 : 0 (11.1 %), C15 : 0 iso 2-OH/C16 : 17c (8.6 %; the MIDI system could not differentiate these two fatty acids) and C13 : 0 (7.3 %). T. ganghwensis (Yi et al., 2004) and T. viridans (Macián et al., 2001a) were also found to contain abundant C15 : 0 iso 2-OH/C16 : 17c (20.6–28.4 %) and C16 : 0 (13.7–22.3 %). However, C17 : 0 and C13 : 0 were present at low levels (0–4.7 %) or were not detectable in these species. Strain TMA1T was rather different from T. loyana (Thompson et al., 2006) in the proportions of C13 : 0 (7.3 vs 1.2 %), C14 : 0 (4.7 vs 13.1 %), C15 : 0 iso 2-OH/C16 : 17c (8.6 vs 31.3 %), C16 : 0 (17.5 vs 4.6 %) and C17 : 0 (11.1 vs 0 %). Other differences in cellular fatty acids between strain TMA1T and Thalassomonas species are shown in Table 1.
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Strain TMA1T grew significantly over a pH range of 7–9, with better growth at pH 8–9. No growth could be observed below pH 6. It grew over a temperature range of 20–35 °C and most rapidly at 25 °C. Growth was relatively slow and weak at 15 and 37 °C and absent at 4, 13 and 40 °C. The strain was halophilic, growing in 1–5 % NaCl, with optimal growth at 3 % NaCl; no growth was observed at 0 or 6–8 % NaCl. Substitution of KCl (1–5 %) for NaCl did not support growth, indicating that the strain required Na+ for growth and that the Na+ requirement was not for osmotic function. Strain TMA1T exhibited good growth in PY, PYN and PYG broth media under aerobic conditions (maximal OD600 >0.6), whereas no growth was observed in these media under anaerobic conditions. This indicated that the strain was a strict aerobe that could not achieve anaerobic growth by either nitrate reduction or glucose fermentation. Various marine bacteria have been reported to grow in CM media and their modifications containing carbohydrates, organic acids or amino acids as sole carbon and energy sources (Shieh et al., 2000, 2003a, b, 2004). Strain TMA1T might require organic growth factors, since it did not grow in any of these media, nor did it grow significantly in any of these media supplemented with Bacto yeast extract at 0.1 g l–1 (maximal OD600 <0.05).
Strain TMA1T was Gram-negative. It produced circular, off-white, opaque and non-luminescent colonies surrounded by distinct depressions on PY agar plates after incubation for 2–5 days. Clear yellow haloes formed around the colonies in contrast to the purple–brown background when the plates were flooded with iodine/potassium iodide solution. This indicated diffusion of agarase out from the colonies and release of reducing compounds during agar hydrolysis. Cells grown in PY broth were straight or curved rods, non-motile and non-flagellated during the late exponential to early stationary phase of growth. Carbohydrate fermentation tests in PYC (Polypepton/yeast extract/carbohydrate) stab media (Shieh et al., 2000) indicated that the strain did not ferment any of the test carbohydrates D-arabinose, L-arabinose, cellobiose, galactose, glucose, lactose, mannose, melibiose, sucrose, trehalose and xylose. Oxidase and catalase tests were both positive. Indole was not produced from tryptophan. Aesculin, alginate, casein, DNA, gelatin and starch were hydrolysed, but lecithin and Tween 80 were not. Nitrate was reduced to nitrite but not further to N2O or N2. Additional phenotypic characterization data are given below in the species description.
Strain TMA1T was phenotypically distinguished from T. ganghwensis (Yi et al., 2004), T. viridans (Macián et al., 2001a) and T. loyana (Thompson et al., 2006) in that it was a non-motile, non-flagellated bacterium capable of decomposing agar. Other characteristics useful for differentiating strain TMA1T from these Thalassomonas species are summarized in Table 2.
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Emended description of the genus Thalassomonas Macián et al. 2001
Thalassomonas (Tha.las'so.mo.nas. Gr. fem. n. thalassa the sea; Gr. n. monas a unit; N.L. fem. n. Thalassomonas a monad from the sea).
Members are Gram-negative rods belonging to the Gammaproteobacteria. Catalase-positive. Oxidase is usually present. Non-motile or motile by means of a single polar flagellum. Halophilic, growing in 2–4 % NaCl but not in the absence of NaCl. Mesophilic, growing at 20–35 °C but not at 4 or 45 °C. Chemo-organotrophs capable of respiratory but not fermentative metabolism. Arginine dihydrolase, lysine decarboxylase and ornithine decarboxylase are absent. Cells contain either C15 : 0 iso 2-OH/C16 : 17c or C16 : 0 as the most abundant fatty acid(s). The DNA G+C content is 39.3–48.5 mol%. The type species is Thalassomonas viridans.
Description of Thalassomonas agarivorans sp. nov.
Thalassomonas agarivorans (a.ga.ri.vo'rans. N.L. n. agarum agar; L. part. adj. vorans devouring, destroying; N.L. part. adj. agarivorans agar-devouring).
In addition to the characteristics included in the emended description of the genus, the following characteristics are observed. Cells during late exponential to early stationary phase of growth in broth cultures are non-motile, straight or curved rods that measure approximately 1.4–2.2 by 0.4–0.7 µm. Colonies produced on agar plates are circular, off-white, opaque, non-luminescent and agarolytic; distinct depressions are formed by these colonies in a few days and much of the agar in the plate medium is liquefied after incubation for several weeks. Growth occurs between 15 and 37 °C with optimal growth at 25 °C; no growth at 4–13 or 40 °C. Growth occurs in 1–5 % NaCl with optimal growth at 3 %; no growth at 0 or 6 % NaCl. Able to grow over a pH range of 7–9 but not at pH 6. Nitrate is reduced to nitrite but not further to N2O or N2. H2S is not produced from thiosulphate. Indole is not produced from tryptophan. Aesculin, alginate, casein, DNA, gelatin and starch are hydrolysed but lecithin, Tween 80 and urea are not. The following constitutive enzyme activities are detected in API ZYM tests: -chymotrypsin, esterase (C4), esterase lipase (C8), N-acetyl--glucosaminidase, -glucosidase, leucine arylamidase, naphthol-AS-BI-phosphohydrolase, acid phosphatase and alkaline phosphatase. Organic growth factors are probably required since growth does not occur on the following compounds as sole carbon sources: glucose, D-arabinose, L-arabinose, cellobiose, fructose, galactose, lactose, maltose, mannose, melibiose, sucrose, trehalose, xylose, glycerol, dulcitol, inositol, mannitol, acetate, citrate, fumarate, -hydroxybutyrate, malonate, tartrate, L-alanine, arginine, aspartate, gluconate, glutamine, glutamate, leucine, lysine, tryptophan and L-aconitate. Cellular fatty acids present at levels greater than 5 % include C16 : 0, C17 : 18c, C17 : 0, C15 : 0 iso 2-OH/C16 : 17c and C13 : 0. Susceptible to ampicillin (10 µg), colistin (10 µg), erythromycin (15 µg), gentamicin (10 µg), kanamycin (30 µg), neomycin (30 µg), novobiocin (30 µg), penicillin G (10 U), polymyxin B (300 U) and tetracycline (30 µg); intermediate susceptibility to nalidixic acid (30 µg); resistant to carbenicillin (100 µg), cephalothin (30 µg), chloramphenicol (30 µg), clindamycin (2 µg), lincomycin (2 µg), oxacillin (1 µg), streptomycin (10 µg) and vancomycin (30 µg).
The type strain, TMA1T (=BCRC 17492T=JCM 13379T), was isolated from shallow seawater of An-Ping Harbour, Tainan, Taiwan. It has a DNA G+C content of 41.0 mol%.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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