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Isolation and Characterization of a Novel Agar-Degrading Marine Bacterium, Gayadomonas Joobiniege Gen, Nov, Sp

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Isolation and Characterization of a Novel Agar-Degrading Marine Bacterium, Gayadomonas Joobiniege Gen, Nov, Sp J. Microbiol. Biotechnol. (2013), 23(11), 1509–1518 http://dx.doi.org/10.4014/jmb.1308.08007 Research Article jmb Isolation and Characterization of a Novel Agar-Degrading Marine Bacterium, Gayadomonas joobiniege gen, nov, sp. nov., from the Southern Sea, Korea Won-Jae Chi1, Jae-Seon Park1, Min-Jung Kwak2, Jihyun F. Kim3, Yong-Keun Chang4, and Soon-Kwang Hong1* 1Division of Biological Science and Bioinformatics, Myongji University, Yongin 449-728, Republic of Korea 2Biosystems and Bioengineering Program, University of Science and Technology, Daejeon 305-350, Republic of Korea 3Department of Systems Biology, Yonsei University, Seoul 120-749, Republic of Korea 4Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology, Daejeon 305-701, Republic of Korea Received: August 2, 2013 Revised: August 14, 2013 An agar-degrading bacterium, designated as strain G7T, was isolated from a coastal seawater Accepted: August 20, 2013 sample from Gaya Island (Gayado in Korean), Republic of Korea. The isolated strain G7T is gram-negative, rod shaped, aerobic, non-motile, and non-pigmented. A similarity search based on its 16S rRNA gene sequence revealed that it shares 95.5%, 90.6%, and 90.0% T First published online similarity with the 16S rRNA gene sequences of Catenovulum agarivorans YM01, Algicola August 22, 2013 sagamiensis, and Bowmanella pacifica W3-3AT, respectively. Phylogenetic analyses demonstrated T *Corresponding author that strain G7 formed a distinct monophyletic clade closely related to species of the family Phone: +82-31-330-6198; Alteromonadaceae in the Alteromonas-like Gammaproteobacteria. The G+C content of strain Fax: +82-31-335-8249; G7T was 41.12 mol%. The DNA-DNA hybridization value between strain G7T and the E-mail: [email protected] phylogenetically closest strain YM01T was 19.63%. The genomes of G7T and YM01T had an average ANIb value of 70.00%. The predominant isoprenoid quinone of this particular strain was ubiquinone-8, whereas that of C. agarivorans YM01T was menaquinone-7. The major fatty T acids of strain G7 were Iso-C15:0 (41.47%), Anteiso-C15:0 (22.99%), and C16:1ω7c/iso-C15:0 2-OH (8.85%), which were quite different from those of YM01T. Comparison of the phenotypic characteristics related to carbon utilization, enzyme production, and susceptibility to antibiotics also demonstrated that strain G7T is distinct from C. agarivorans YM01T. Based on its phenotypic, chemotaxonomic, and phylogenetic distinctiveness, strain G7T was considered a novel genus and species in the Gammaproteobacteria, for which the name Gayadomonas joobiniege gen. nov. sp. nov. (ATCC BAA-2321 = DSM25250T = KCTC23721T) is proposed. pISSN 1017-7825, eISSN 1738-8872 Copyright© 2013 by Keywords: Agarase, Alteromonadaceae, Alteromonas-like Gammaproteobacteria, agar degradation, The Korean Society for Microbiology Gayadomonas joobiniege and Biotechnology Introduction antioxidant activity, therapeutic activity in inflammatory disease, and antitumor activity, etc. [3, 11, 19], which may Marine microorganisms have received a great deal of broaden its application in the food, cosmetic, and attention in various efforts to utilize the abundant biological pharmaceutical industries as well as biorefinement or resources in the sea. One of these resources is agar, which biofuel industries. is a major component of red algae [6]. Agar is widely used For an efficient hydrolysis of agar, research seeking a as a dietary ingredient in food and as a gelling agent in good agarase has been under intense spotlight. A number solid culture media for microbial growth. Recently, agar of microorganisms with agar-hydrolyzing activity, such as oligosaccharides have also been reported to have Pseudoalteromonas marinoglutinosa [30], Alteromonas atlantica November 2013 ⎪ Vol. 23⎪ No. 11 1510 Chi et al. [1], Glaciecola mesophila [31], Catenovulum agarivorans [37], and Thalassomonas agarivorans [18], which are classified as Alteromonas-like Gammaproteobacteria [14, 16], have been isolated from marine environments. We recently isolated another Alteromonas-like marine bacterium (designated as strain G7T), which can grow on minimal medium supplemented with agar as the sole carbon source at higher temperature (above 40oC). Genomic sequencing of G7T revealed that it had many genes encoding hydrolytic enzymes: 50 sulfatases, 17 glycoside hydrolases, 13 agarases, 8 β-galactosidases, 3 altronate hydrolases, and 1 cellulase, which may act in the complete hydrolysis of sulfated algal polysaccharides [24]. Because of the great potential for the bacterium to be used as a bioresource for bioconversion of algal polysaccharides, we used a polyphasic taxonomic approach for the classification of strain G7T. This report describes the characteristics of the G7T strain as a novel genus of the family Alteromonadaceae. Materials and Methods Chemicals Agar and agarose were purchased from Amresco Inc. (USA) and Takara Shuzo Inc. (Japan), respectively. All other chemicals were purchased from Sigma Chemical Co. (USA). Fig. 1. Agarase production by strain G7T. (A) Detection of agarolytic activity of strain G7T on agar plate. The Isolation of Agarase-Producing Microorganisms strain was cultured on an ASW-YP agar plate at 40oC for 2 days (left), Coastal seawater of Gaya Island, Republic of Korea, was and Lugol’s iodine solution was overlaid to detect reducing sugars collected to isolate agar-degrading bacteria. The collected sample and degraded product from agar by agarase (right). (B) Cell growth was serially diluted from 10-1 to 10-5, and 200 µl of each dilution and agarase production of strain G7T in ASW-YP broth depending on was smeared on an artificial seawater (ASW) agar plate [20] cultivation time. The agarolytic activity was estimated by the colorimetric containing 1.0% yeast extract (w/v) and 0.3% bacto peptone (w/v) DNS method to measure the reducing sugar that resulted from (ASW-YP), and was incubated aerobically at 40oC for 24 h. The hydrolysis of agar as the substrate. Each value is an average of three ● ● ■ ■ ASW contained 6.1 g Tris base, 12.3 g MgSO4, 0.74 g KCl, 0.13 g parallel replicates. - , Cell growth; - , agarase activity. (NH4)2HPO4, 17.5 g NaCl, and 0.14 g CaCl2 dissolved in 1 L of distilled water. A total of 1,136 colonies were collected and o transferred to fresh ASW-YP plates and incubated at 40 C for 24 h. at regular time intervals, and the optical density (OD) was The plate was stained with Lugol’s iodine solution (0.05 M iodine measured at 600 nm (OD600) to plot the growth curve. The sample in 0.12 M KI) to detect agarase activity (Fig. 1A). Colonies with was centrifuged at 14,000 rpm for 10 min and its supernatant was high agarase activity were isolated from the replica plate and collected to measure agarase activity. A substrate solution containing transferred to a fresh ASW-YP plate. The bacterial colonies were 0.2% agarose in 10 mM Tris-HCl (pH 8.0) was used for the agarase streaked five times to obtain a single colony for pure culture. One reaction. Agarase activity was measured by the previously marine bacterium with agar-hydrolyzing activity was selected described method [27] using 3,5-dinitrosalicylic acid (DNS). One T and designated as strain G7 in this study. After incubation in unit (U) of agarase was defined as the amount of enzyme that o ASW-YP broth at 40 C for 1 day, the culture was supplemented produced 1 µmol galactose per minute at 40oC. Galactose was used o with 10% glycerol (w/v) and stored at -80 C as the stock culture. as a reference reducing sugar for preparing the standard curve. T Production of Agarase by Strain G7 16S rRNA Sequencing and Construction of Phylogenetic Tree T Cell growth and agarase activity of strain G7 were observed by The bacterial strain was cultured in ASW-YP liquid medium for incubating it in ASW-YP liquid medium containing 0.1% agar (w/v) 3 days, and genomic DNA was extracted with a genomic DNA o at 40 C for 72 h (Fig. 1B). Then, 1 ml of culture broth was sampled extraction kit (Promega Co., USA). The 16S rRNA gene was J. Microbiol. Biotechnol. Gayadomonas joobiniege gen. nov. sp. nov. 1511 amplified by PCR using universal bacterial primers (27F, 5’- To determine antibiotic susceptibility, strain G7T and C. agarivorans AGAGTTTGATCCTGGCTCAG-3’; and 1492R, 5’-TACCTTGTT YM01 were smeared on ASW-YP agar plates and incubated at ACGACTT-3’), and nucleotide sequencing was performed using 40oC for 1 h. Paper discs containing 30 µl of thiostrepton (100 µg/ml), an Applied Biosystems 3730xl DNA Analyzer. Analysis of the 16S kanamycin (100 µg/ml), neomycin (100 µg/ml), ampicillin (100 µg/ml), rRNA gene sequence revealed that strain G7T belongs to the class apramycin (100 µg/ml), and chloramphenicol (100 µg/ml) were Gammaproteobacteria. The 16S rRNA gene sequences of type strains placed on the smear plate. The plates were incubated at 40oC for related to strain G7T were collected from the EzTaxon server 24 h and the zone of inhibition surrounding each antibiotic disc (http://www.eztaxon.org; [9]). The 16S rRNA sequences were was measured. aligned using ClustalW software [35], and the 5’ and 3’ gaps were edited using the BioEdit program [13]. Neighbor-joining (NJ), Chemotaxonomic Characteristics maximum likelihood (ML), and maximum parsimony (MP) methods The major respiratory quinones of strain G7T and C. agarivorans from the PHYLIP suite program [12] were used to construct the YM01 were analyzed by reverse-phase high-performance liquid phylogenetic tree. The bootstrap value was calculated using data chromatography (HPLC) after growth on Marine Broth (MB; Difco) restructured nearly 1,000 times and marked into the branching plates [23]. Cellular fatty acid methyl ester (FAME) mixtures were point. The evolutionary distance matrix was estimated according prepared from G7T and YM01 cells grown on MB (Difco) plates for to Kimura’s 2-parameter model [21].
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