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Aliagarivorans Marinus Gen. Nov., Sp. Nov. and Aliagarivorans Taiwanensis Sp

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Aliagarivorans Marinus Gen. Nov., Sp. Nov. and Aliagarivorans Taiwanensis Sp International Journal of Systematic and Evolutionary Microbiology (2009), 59, 1880–1887 DOI 10.1099/ijs.0.008235-0 Aliagarivorans marinus gen. nov., sp. nov. and Aliagarivorans taiwanensis sp. nov., facultatively anaerobic marine bacteria capable of agar degradation Wen Dar Jean,1 Ssu-Po Huang,2 Tung Yen Liu,2 Jwo-Sheng Chen3 and Wung Yang Shieh2 Correspondence 1Center for General Education, Leader University, No. 188, Sec. 5, An-Chung Rd, Tainan, Wung Yang Shieh Taiwan, ROC [email protected] 2Institute of Oceanography, National Taiwan University, PO Box 23-13, Taipei, Taiwan, ROC 3College of Health Care, China Medical University, No. 91, Shyue-Shyh Rd, Taichung, Taiwan, ROC Two agarolytic strains of Gram-negative, heterotrophic, facultatively anaerobic, marine bacteria, designated AAM1T and AAT1T, were isolated from seawater samples collected in the shallow coastal region of An-Ping Harbour, Tainan, Taiwan. Cells grown in broth cultures were straight rods that were motile by means of a single polar flagellum. The two isolates required NaCl for growth and grew optimally at about 25–30 6C, in 2–4 % NaCl and at pH 8. They grew aerobically and could achieve anaerobic growth by fermenting D-glucose or other sugars. The major isoprenoid quinone was Q-8 (79.8–92.0 %) and the major cellular fatty acids were summed feature 3 (C16 : 1v7c and/or iso-C15 : 0 2-OH; 26.4–35.6 %), C18 : 1v7c (27.1–31.4 %) and C16 : 0 (14.8–16.3 %) in the two strains. Strains AAM1T and AAT1T had DNA G+C contents of 52.9 and 52.4 mol%, respectively. The two strains had a 16S rRNA gene sequence similarity of 98.6 % and shared 84.9–92.4 % sequence similarity with the type strains of Agarivorans albus (91.2– 92.4 %), eight Alteromonas species (84.9–87.1 %), two Aestuariibacter species (86.0–87.0 %), Bowmanella denitrificans (86.1–86.7 %), eight Glaciecola species (85.0–87.9 %) and Salinimonas chungwhensis (85.9–86.1 %). Despite their high sequence similarity, strains AAM1T and AAT1T had a DNA–DNA relatedness value of only 4.5 %. The data obtained from these polyphasic taxonomic studies revealed that the two agarolytic isolates could be classified as representatives of two novel species in a new genus, Aliagarivorans gen. nov., with Aliagarivorans marinus sp. nov. [type strain is AAM1T (5BCRC 17888T5JCM 15522T)] as the type species and Aliagarivorans taiwanensis sp. nov. [type strain is AAT1T (5BCRC 17889T5JCM 15537T)] as a second species. Agar, a complex polysaccharide extracted from marine red and ‘Verrucomicrobia’ (Scheuermayer et al., 2006; Shieh & algae, is widely used as a gelling agent for microbiological Jean, 1998). culture media. Hydrolysis of this refractory material, a Two strains of agarolytic bacteria, AAM1T and AAT1T, property found only among members of the domain were isolated in our laboratory from seawater samples ‘Bacteria’, is indicated by the development of softening, collected in the shallow coastal region of An-Ping Harbour, depressions or, in some cases, complete liquefaction of the Tainan, Taiwan, during a survey of the diversity of marine agar surrounding colonies of agarolytic bacteria. Marine agarolytic bacteria in Taiwan. Data from the present agarolytic bacteria are ubiquitous in coastal and estuarine polyphasic study indicated that the two isolates could be regions. They include species of various genera belonging classified as representatives of two different species in a to the phyla ‘Bacteroidetes’ (previously known as the Cytophaga–Flavobacterium–Bacteroides) (Yoon et al., new genus belonging to the class Gammaproteobacteria. 2007), ‘Proteobacteria’ (Jean et al., 2006a; Shieh et al., 2008) An-Ping Harbour is located in the south-west coast of Taiwan. Seawater samples were collected from the shallow The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene T T coastal regions of this harbour in the morning at low tide. sequences of strains AAM1 and AAT1 are FJ167390 and FJ167391, Each sample was decimally diluted to the order of 1023 respectively. 1880 008235 G 2009 IUMS Printed in Great Britain Aliagarivorans gen. nov. with two novel species with sterile NaCl-Tris buffer (30 g NaCl and 0.24 g Tris Gammaproteobacteria and were rather closely related to base in 1 l deionized water, pH 8.0). Aliquots (0.1 ml) of each other (98.6 % sequence similarity, 21 differences out the 10-fold dilutions (1021 to 1023) were spread onto of 1461 nt positions) than to strains of any recognized polypeptone-yeast extract (PY) plate medium (Shieh et al., bacterial species (,93 % sequence similarity). Strains 2000) in triplicate. The plates were incubated at 25 uCin AAM1T and AAT1T showed highest levels of sequence the dark for 7 days under aerobic conditions. Individual similarity to the type strains of Agarivorans albus (91.2– colonies that appeared to be agarolytic were picked off and 92.4 %; Kurahashi & Yokota, 2004), eight Alteromonas purified by successive streaking on PY plates. Maintenance species (84.9–87.1 %; Bowman & McMeekin, 2005; Chiu et of the isolates in our laboratory was performed regularly at al., 2007; Ivanova et al., 2005; Martı´nez-Checa et al., 2005; intervals of 3–4 months by inoculating early stationary Van Trappen et al., 2004a; Yoon et al., 2003, 2004), two phase cultures grown in PY broth into 7/10-strength Aestuariibacter species (86.0–87.0 %; Yi et al., 2004), seawater at a ratio of 1 : 25 (v/v). Maintenance cultures Bowmanella denitrificans (86.1–86.7 %; Jean et al., 2006c), were kept at 20 uC under aerobic conditions. Lyophilized eight Glaciecola species (85.0–87.9 %; Baik et al., 2006; cultures of both strains were also created. Bowman et al., 1998; Matsuyama et al., 2006; Romanenko Physiological and morphological characterization of et al., 2003; Yong et al., 2007; Van Trappen et al., 2004b; AAM1T and AAT1T, including growth and other pheno- Zhang et al., 2006) and Salinimonas chungwhensis (85.9– typic properties, was carried out according to previously 86.1 %; Jeon et al., 2005). The distant relationship between described established procedures (Jean et al., 2006b), with the two novel isolates and these bacteria was also evident in modifications and additional tests as described below. the neighbour-joining tree, in which the two isolates Hydrolysis of chitin and cellulose was tested by growth of formed a stable monophyletic clade (bootstrap value, the strains on modified PY plate media containing either 100 %) located next to a sister clade comprising only 21 Agarivorans albus strains (Fig. 1). The two isolates and colloidal chitin or cellulose at 2 g l (Shieh et al., 2008). T Haemolysis was tested as described by Chiu et al. (2007). Agarivorans albus (strain MKT 106 plus other reference Utilization of various compounds as sole carbon and strains), together with the type strains of various other energy sources for growth was tested in carbohydrate/ species belonging to the Alteromonadaceae (eight mineral (CM) media (Shieh et al., 2004) plus various Alteromonas species, eight Glaciecola species, two carbon sources. Sugars and sugar alcohols were both Aestuariibacter species, S. chungwhensis and B. denitrificans) provided at 5 g l21, whereas organic acids and amino acids formed a suprageneric monophyletic clade (Fig. 1). Similar were each provided at 2 g l21. All the test cultures were results were obtained from the maximum-likelihood and incubated aerobically at 30 uC in the dark for 7 days, unless maximum-parsimony algorithms (not shown). The low stated otherwise. levels of 16S rRNA gene sequence similarity to all recognized bacterial species (,93 %), together with the Cells grown in PY broth and on PY plate medium at 30 uC phylogenetic data from the three tree-making algorithms for 7 days were used for analyses of cellular fatty acids, employed, showed that the two novel isolates could be + isoprenoid quinones and DNA G C content according to assigned to a novel genus. the methods described by Shieh et al. (2008). DNA–DNA T T hybridization between strains AAM1Tand AAT1T was Strains AAM1 and AAT1 , like Agarivorans albus and performed as described by Jean et al. (2009). species of the genera Alteromonas, Glaciecola, Aestuariibacter, Salinimonas and Bowmanella, contained Cells grown in PY broth at 30 uC for 7 days were harvested [ summed feature 3 C16 : 1v7c and/or iso-C15 : 0 2-OH (the by centrifugation. Extraction and purification of total two fatty acids could not be differentiated in the MIDI genomic DNA from the cells and PCR amplification of 16S system); 26.4–35.6 % of the total fatty acids],C v7c rRNA genes were performed according to previously 18 : 1 (27.1–31.4 %) and C16 : 0 (14.8–16.3 %) as the major fatty described methods (Jean et al., 2006b). Sequencing of the acids (Table 1). However, the fatty acid profiles of the two 16S rRNA genes, alignment and comparison of the novel isolates could be distinguished from those of closely resulting sequences with reference sequences available in related species by differences in the levels of the fatty acids GenBank, calculation of distance matrices for the aligned C18 : 1v7c (27.1–31.4 % vs 0–19.4 %), iso-C18 : 0 (1.1–6.1 % sequences and reconstruction of phylogenetic trees based vs 0 % to trace amount detected, with the exception of on the neighbour-joining, maximum-parsimony and Alteromonas addita) and iso-C16 : 0 (2.8–6.5 % vs 0–1.5 %, maximum-likelihood methods were performed as with the exception of Agarivorans albus). Other quantitat- described by Shieh et al. (2004) and Jean et al. (2006b). ive differences in the fatty acids that might serve to Stability of clusters was evaluated by bootstrap analysis of differentiate the two novel isolates from the relevant species 1000 resamplings. are listed in Table 1.
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