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1 Institute of Oceanography, National Taiwan University, PO Box 23-13, Taipei, Taiwan
2 National Center for Ocean Research, National Taiwan University, PO Box 23-13, Taipei, Taiwan
3 GBF – Gesellschaft für Biotechnologische Forschung, Mascheroder Weg 1, D-38124 Braunschweig, Germany
Correspondence
Wung Yang Shieh
winyang{at}ntu.edu.tw
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7c and/or iso-C15 : 0 2-OH (22.4–33.7 %), C16 : 0 (19.0–22.7 %) and C18 : 17c (11.3–11.7 %) as the major fatty acids. Strains AT1T and AS1T had DNA G+C contents of 43.1 and 45.3 mol%, respectively. Phylogeny based on 16S rRNA gene sequences, together with data from morphological, physiological and chemotaxonomic characterization, indicated that the two isolates could be classified as representatives of two novel species in the genus Alteromonas, for which the names Alteromonas tagae sp. nov. (type strain AT1T=BCRC 17571T=JCM 13895T) and Alteromonas simiduii sp. nov. (type strain AS1T=BCRC 17572T=JCM 13896T) are proposed.
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). The major form of mercury in the atmosphere is elemental mercury (Hg0), which is volatile and is oxidized to the mercuric ion (Hg2+) as a result of its interaction with ozone in the presence of water (Munthe, 1992). Thus, most of the mercury entering the aquatic environment is Hg2+. Inorganic mercury species, Hg2+ and Hg0, present in the aquatic environment are subjected to microbiological conversion to highly toxic methyl mercury compounds that are subsequently bioaccumulated through the food chain. The health of predatory organisms at the top of the food chain, such as fish, birds and humans, is thereby threatened (Muir et al., 1999).
Mercury-resistant bacteria are usually aerobes or facultative anaerobes, which are readily isolated on a variety of media from water, soil and sediment as well as from humans and other animals (Osborn et al., 1997; Barkay et al., 2003). They play a major role in the global cycling of mercury. The mechanism of their mercury resistance is mediated by cytoplasmic mercuric reductase, which converts soluble Hg2+ to insoluble Hg0, followed by volatilization of the relatively non-toxic Hg0; the mercuric reductase is encoded by the merA gene (Silver & Phung, 1996). Various genera such as Acinetobacter, Aeromonas, Alcaligenes, Azotobacter, Bacillus, Bacteriodes, Beijerinckia, Caulobacter, Chromobacterium, Citrobacter, Clostridium, Enterobacter, Erwinia, Escherichia, Exiguobacterium, Flavobacterium, Klebsiella, Moraxella, Morganella, Mycobacterium, Paracoccus, Proteus, Pseudoalteromonas, Pseudomonas, Rhodococcus, Salmonella, Serratia, Shewanella, Shigella, Staphylococcus, Streptococcus, Streptomyces, Thiobacillus, Xanthomonas and Yersinia are reported to include mercury-resistant bacteria (Ji et al., 1989; Osborn et al., 1997; Barkay et al., 2003). Among them only Pseudoalteromonas haloplanktis and some Caulobacter strains are considered to be autochthonous marine bacteria due to the requirement of NaCl for growth.
Two marine mercury-resistant isolates were recovered from water samples collected from the Er-Jen River estuary, Tainan, Taiwan. Polyphasic characterization data from this study indicated that the two isolates should be classified as the type strains of two novel species in the genus Alteromonas.
Polypeptone–yeast extract–mercury (PYM) broth media used for selective cultivation of mercury-resistant bacteria were made up of two parts. Part I contained 3 g polypeptone (Nihon Seiyaku), 1 g Bacto yeast extract (Difco), 25 g NaCl and 2 g MgCl2.6H2O dissolved in 900 ml deionized water and adjusted to pH 8.0. Part II contained 2.7–13.5 mg (approximately 10–50 µmol) HgCl2 dissolved in 100 ml deionized water. The two parts were autoclaved separately and mixed at room temperature. Other culture media used for the present study were as described by Shieh et al. (2000), while polypeptone–yeast extract (PY) broth and its derivatives were modified with MgCl2.6H2O at 2 g l–1 and were adjusted to pH 8.0.
The Er-Jen River is located in south-west Taiwan, and is notorious for severe heavy-metal pollution by some unregulated metal reclamation processing sites at the downstream area since the 1970s. Water samples that had salinities of 14.0–34.6 psu were collected from a shallow estuarine region of the river. Each sample was diluted 10-fold with sterile NaCl/Tris buffer (30 g NaCl and 0.24 g Tris in 1 litre deionized water, pH 8.0). Portions (1 ml) of the water samples and their dilutions (10- to 100-fold) were transferred to culture tubes containing PYM broth (10 ml). All culture tubes were incubated aerobically at 30 °C in the dark for 7 days. Cultures that developed visible turbidity were streaked (one loopful) on PY plate medium. Individual colonies appearing on each of the plates were picked off and purified by successive streaking on PY plates. PY stab cultures of the isolates were maintained at 25 °C under aerobic conditions. Strains AT1T and AS1T, two of the isolates deposited in both the Japan Collection of Microorganisms (JCM) and the Bioresource Collection and Research Center (BCRC) as lyophilized cultures, were used for the present study.
Strains AT1T and AS1T were grown in PY broth at 30 °C and at the early stationary phase were inoculated (0.1 ml) into tubes containing 10 ml PYM broth with approximately 44 µM HgCl2, in order to determine mercury-resistant growth and mercury-reducing activity. All culture tubes were sealed with rubber stoppers and incubated statically at 30 °C. Bacterial growth was monitored daily according to OD600 readings by using a Spectronic Instruments 20D+ spectrophotometer. Before mercury measurement, the converted Hg0 remaining in each culture was removed by purging for 5 min with a high-purity N2 gas. Residual mercury was measured after chemical digestion with BrCl by UV oxidation, followed by NH2OH.HCl pre-reduction and SnCl2 reduction (Bloom & Crecelius, 1983). Total mercury analysis was carried out daily for up to 4 days by an online purge and trap system combined with flow-injection and gold amalgamation pre-concentration techniques, together with cold vapour atomic fluorescence detection (Tseng et al., 2003). Instrument calibration was performed before and during sample analysis by injection of a Hg0 vapour standard of known mass into the argon gas stream and the bubbler, a gas–liquid separator. The relative standard deviation of replicate samples, a measure of overall precision, was less than 5 % (n=3). Recovery from analytical spikes averaged 100±5 % (n=10). All experimental steps were in the dark when possible and were in compliance with the ultraclean techniques of Tseng et al. (2003) throughout the procedure. All data presented here represent the means of at least three replicates.
Physiological and morphological characteristics of strains AT1T and AS1T were determined following the established procedures described in our recent report (Jean et al., 2006a) with modifications and additional tests as described below. Haemolysis was tested by growing cells on blood-agar plates (6.5 % sheep blood; Creative Microbiologicals) that had been spread with sterile NaCl/Tris buffer (0.1 ml). Hydrolysis of chitin was tested by growth of the strains on a modified PY plate medium containing colloidal chitin (Hobel et al., 2005) at 2 g l–1. Besides the cells grown in PY broth, colonies produced on PY plate medium at 20 or 28 °C for 3 days or more were also used for observation of prosthecae and buds via transmission electron microscopy (Bouchotroch et al., 2001; Van Trappen et al., 2004). All the test cultures were incubated aerobically at 30 °C in the dark for 7 days, unless stated otherwise.
Strains AT1T and AS1T were cultivated aerobically in PY broth at 30 °C in the dark for 2 days. The cultures were centrifuged to harvest cell mass for analysis. Polar lipids in the cells were extracted, purified and analysed by the methods described by Lin & Shieh (2006). Isoprenoid quinones were extracted, purified and analysed by using an HPLC apparatus equipped with a reversed-phase column (Jean et al., 2006b). Fatty acids in whole cells grown on PY plate medium at 30 °C for 2 days were extracted, saponified and esterified, followed by GC analysis of the fatty acid methyl esters according to the instructions of the MIDI system (Sasser, 1997). This work was performed at the BCRC, Food Industry Research and Development Institute, Taiwan. Determination of the DNA G+C content by HPLC analysis (Shieh & Liu, 1996) was also performed at the BCRC.
Cells grown in PY broth at 30 °C for 2 days were harvested by centrifugation. Extraction and purification of total genomic DNA from the cells and PCR amplification of 16S rRNA genes followed the methods described by Jean et al. (2006a). Sequencing of the 16S rRNA genes, alignment and comparison of the resulting sequences with reference sequences available in the GenBank database, calculation of distance matrices for the aligned sequences and reconstruction of phylogenetic trees by the neighbour-joining, maximum-parsimony and maximum-likelihood methods were performed as described in our recent reports (Shieh et al., 2004; Jean et al., 2006a). The stability of clusters was evaluated by a bootstrap analysis of 1000 replications.
Strains AT1T and AS1T grew in PY broth over a pH range of 6–9, and most rapidly at pH 7–8. No growth was observed at pH 5. The two strains grew in PY broth over a temperature range of 15–40 °C, with an optimum at about 30 °C. Only strain AS1T grew at 10 °C within 15–20 days of incubation. Neither of the strains grew at 4 or 42–45 °C. The two strains were halophilic bacteria that grew well in PY broth at NaCl levels of 0.5–12 % (maximal OD600 >0.5), with optimum growth at 2–4 % NaCl. No growth was observed at 0 or 14–15 % NaCl. Strain AT1T grew at 13 % NaCl within 5–10 days of incubation (maximal OD600 >0.3) but strain AS1T did not; weak growth was observed for strain AS1T after incubation for 15–20 days (maximal OD600 <0.1). Strains AS1T and AT1T were mercury-resistant bacteria. They grew significantly in PYM broth containing HgCl2 at an initial concentration of about 44 µM. Mercury-resistant growth was accompanied by a rapid decrease in Hg2+ concentration (>20 µM) within 3 days (Fig. 1). Strains AT1T and AS1T could have reduced Hg2+ to Hg0 during this growth.
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), 304 (A), 734 (A), 736 (T), 770 (T) and 809 (A), were also present in these sequences. Moreover, phylogeny based on neighbour-joining analysis of 16S rRNA gene sequences revealed that the closest neighbours of strains AT1T and AS1T were species of the genus Alteromonas in the family Alteromonadaceae (Fig. 2). Similar results were obtained with the maximum-parsimony and maximum-likelihood algorithms (data not shown). Strains AT1T and AS1T showed, respectively, 93.9–95.8 and 95.3–96.8 % 16S rRNA gene sequence similarity to the type strains of the six recognized Alteromonas species. The next closest neighbours of strains AT1T and AS1T were species of the genera Aestuariibacter (90.5–93.5 % sequence similarity) and Salinimonas (91.5–91.7 %) in the family Alteromonadaceae. No other species shared more than 91 % sequence similarity with the two novel strains.
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7c and/or iso-C15 : 0 2-OH (22.4–33.7 %; the two fatty acids could not be differentiated in the MIDI system) and C18 : 17c (11.3–11.7 %) as the major cellular fatty acids. The remaining cellular fatty acids are listed in Table 1. Quantitative differences in the fatty acids can be used to differentiate the two strains from recognized species of the genus Alteromonas despite the different cultivation conditions used. The polar lipids of strain AT1T consisted of phosphatidylethanolamine (46.6 %), phosphatidylglycerol (28.9 %) and sulfolipid (24.5 %), whereas in strain AS1T they consisted of phosphatidylethanolamine (48.2 %) and phosphatidylglycerol (51.8 %). Some Alteromonas species, such as Alteromonas addita and Alteromonas macleodii, were also found to have phosphatidylethanolamine and phosphatidylglycerol as major polar lipids (Ivanova et al., 2000, 2005). Strains AT1T and AS1T contained Q-8 as the predominant isoprenoid quinone (99.9 % for AT1T and 91.3 % for AS1T), but only AS1T contained Q-4 (4.3 %) and Q-6 (4.3 %). Q-8 was detected as the predominant isoprenoid quinone in Alteromonas hispanica (96.5 %; Martínez-Checa et al., 2005), Alteromonas macleodii (92 %; Yoon et al., 2003), Alteromonas marina (94 %; Yoon et al., 2003) and Alteromonas litorea (Yoon et al., 2004). However, Q-4 and Q-6 have not been detected in these Alteromonas species.
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; Martínez-Checa et al., 2005). Both strains AT1T and AS1T were also found to produce buds and prosthecae (Figs 3 and 4). They shared many other phenotypic characteristics. The two, however, could be differentiated from each other by different colony types and by different reactions in tests for hydrolysis of casein, lecithin and starch, activity of cystine arylamidase and 
-galactosidase, reduction of nitrate to nitrite, growth at 10 °C, growth on D-fructose as a sole carbon and energy source and sensitivity to the vibriostatic agent O/129.
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shows characteristics that are useful for differentiation between the two novel species and the other recognized species of the genus Alteromonas. Detailed characterization data are given below in the species descriptions.
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Description of Alteromonas tagae sp. nov.
Alteromonas tagae (ta'gae. N.L. gen. n. tagae of Taga, named after Nobuo Taga, a pioneering Japanese marine microbiologist).
Cells are Gram-negative rods (1.2–2.5x0.5–0.9 µm) that are motile by means of a single polar flagellum. Colonies produced on PY agar plates at 30 °C for 72–96 h are approximately 2.0–3.5 mm in diameter, cream-coloured, opaque, of low convexity and non-luminescent, with somewhat undulatory edges. Swarming does not occur. Buds and prosthecae are commonly produced on cells grown on PY agar plates at 20 or 28 °C for 3–7 days; these structures can also be observed on cells grown in PY broth at 30 °C for 3–7 days. Extracellular bleb-like structures are produced. Endospores are absent. Chemo-organotroph capable of respiratory, but not fermentative, metabolism. Sodium ions are required for growth; growth occurs at NaCl levels of 0.5–13 %, with an optimum at 2–4 % and no growth at 0 or 14–15 % NaCl. Growth occurs at 15–40 °C, with optimum growth at about 30 °C; no growth at 4–10 or 42–45 °C. Able to grow over a pH range of 6–9 but not at pH 5. Acid is not produced from oxidation or fermentation of the following carbohydrates: D-glucose, D-arabinose, L-arabinose, D-cellobiose, D-galactose, D-lactose, D-maltose, D-mannose, D-melibiose, sucrose, D-trehalose, D-xylose, dulcitol, inositol or D-mannitol. Able to reduce Hg2+ to Hg0. Poly-
-hydroxybutyrate is accumulated as an intracellular reserve product. Negative for denitrification and haemolysis tests. Nitrate is not reduced to nitrite. Indole is not produced from tryptophan. H2S is not produced from thiosulfate. Oxidase and catalase are present, but arginine dihydrolase, lysine decarboxylase and ornithine decarboxylase are absent. Aesculin, alginate, casein, DNA, gelatin, lecithin, starch, and Tweens 20 and 80 are hydrolysed but agar, chitin and urea are not. Able to grow on the following compounds as sole carbon and energy sources: D-cellobiose, D-glucose, D-galactose, D-lactose, D-melezitose, D-melibiose, D-ribose, sucrose, D-trehalose, glycerol, acetate, -hydroxybutyrate, L-lactate, L-alanine, L-glutamic acid and L-threonine. Unable to grow on the following compounds as sole carbon and energy sources: D-arabinose, L-arabinose, D-fructose, D-mannose, D-xylose, dulcitol, inositol, D-mannitol, D-sorbitol, citrate, fumarate, malonate, tartrate and D-arginine. The following constitutive enzyme activities are detected in API ZYM tests: leucine arylamidase, valine arylamidase, esterase (C4), esterase lipase (C8), lipase (C14), acid phosphatase, alkaline phosphatase and naphthol-AS-BI-phosphohydrolase. Polar lipids comprise phosphatidylethanolamine (46.6 %), phosphatidylglycerol (28.9 %) and sulfolipid (24.5 %). Q-8 is the only isoprenoid quinone (99.9 %) but trace amounts of some others may also occur. Cellular fatty acids present at levels greater than 3 % include C16 : 17c and/or iso-C15 : 0 2-OH (22.4 %), C16 : 0 (19.0 %), C18 : 17c (11.7 %), C17 : 18c (9.4 %), C17 : 0 (8.2 %), and iso-C16 : 1 I and/or C14 : 0 3-OH (3.9 %). Sensitive to the vibriostatic agent O/129 at 150 µg. Susceptible to ampicillin (10 µg), chloramphenicol (30 µg), colistin (10 µg), carbenicillin (100 µg), erythromycin (15 µg), gentamicin (10 µg), kanamycin (30 µg), nalidixic acid (30 µg), neomycin (30 µg), novobiocin (30 µg), polymyxin B (300 U), streptomycin (10 µg) and tetracycline (30 µg), and intermediately susceptible to vancomycin (30 µg). Resistant to cephalothin (30 µg), clindamycin (2 µg), lincomycin (2 µg), oxacillin (1 µg) and penicillin G (10 U). The DNA G+C content is 43.1 mol%.
The type strain, AT1T (=BCRC 17571T=JCM 13895T), was isolated from a water sample collected at the estuary of the Er-Jen River, Tainan, Taiwan.
Description of Alteromonas simiduii sp. nov.
Alteromonas simiduii (si.mi'du.i.i. N.L. gen. n. simiduii of Simidu, named after Usio Simidu, a Japanese microbiologist, for his work on marine microbiology).
Description is as for the species description of Alteromonas tagae with the following differences. Cells are 1.2–2.5 µm long and 0.4–0.8 µm wide. Colonies produced on PY agar plates at 30 °C for 72–96 h are approximately 1–3 mm in diameter, off-white, translucent, umbonate and non-luminescent, with somewhat undulatory edges. Growth occurs in PY broth at 10 °C within 15–20 days incubation. Growth occurs at NaCl levels of 0.5–13 %; growth is slow and weak at 13 % NaCl. Casein, lecithin and starch are not hydrolysed. D-Fructose can be utilized as a sole carbon and energy source for growth. Nitrate is reduced to nitrite. Cystine arylamidase and -galactosidase are present in API ZYM tests. Polar lipids comprise phosphatidylethanolamine (48.2 %) and phosphatidylglycerol (51.8 %). Isoprenoid quinones comprise Q-8 (91.3 %), Q-4 (4.3 %) and Q-6 (4.3 %). Cellular fatty acids present at levels greater than 3 % include C16 : 17c and/or iso-C15 : 0 2-OH (33.7 %), C16 : 0 (22.7 %), C18 : 17c (11.3 %), C14 : 0 (5.7 %) and C17 : 18c (4.5 %). Resistant to the vibriostatic agent O/129 at 150 µg. Resistant to vancomycin (30 µg). The DNA G+C content is 45.3 mol%.
The type strain, AS1T (=BCRC 17572T=JCM 13896T), was isolated from a water sample collected at the estuary of the Er-Jen River, Tainan, Taiwan.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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