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J. Gen. Appl. Microbiol., 55(2): 147-153(2009)

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J. Gen. Appl. Microbiol., 55(2): 147-153(2009) J. Gen. Appl. Microbiol., 55, 147‒153 (2009) Full Paper Chitiniphilus shinanonensis gen. nov., sp. nov., a novel chitin-degrading bacterium belonging to Betaproteobacteria Kazuaki Sato,1 Yuichi Kato,1 Goro Taguchi,1 Masahiro Nogawa,1 Akira Yokota,2 and Makoto Shimosaka1,* 1 Division of Applied Biology, Faculty of Textile Science and Technology, Shinshu University, Ueda, Nagano 386‒8567, Japan 2 Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113‒0032, Japan (Received September 2, 2008; Accepted December 22, 2008) A bacterial strain capable of degrading chitin, strain SAY3T, was isolated from moat water of Ueda Castle in Nagano Prefecture, Japan. The strain was gram-negative, curved rod-shaped, facultatively anaerobic, and motile with a single polar fl agellum. It grew well with chitin as a sole carbon source. The cellular fatty acids profi les showed the presence of C16:1 ω7c and C16:0 as the major components. The G+C content of DNA was 67.6 mol% and Q-8 was the major respira- tory quinone. A 16S rRNA gene sequence-based phylogenetic analysis showed the strain be- longed to the family Neisseriaceae but was distantly related (＜94% identity) to any previously known species. Since the strain was clearly distinct from closely related genera in phenotypic and chemotaxonomic characteristics, it should be classifi ed under a new genus and a new spe- cies. We propose the name Chitiniphilus shinanonensis gen. nov., sp. nov. The type strain is SAY3T (=NBRC 104970T=NICMB 14509T). Key Words—Betaproteobacteria; chitin; Chitiniphilus shinanonensis gen. nov., sp. nov.; chitinolytic bacterium; Neisseriaceae; 16S rRNA gene sequence Introduction (Cohen-Kupiec and Chet, 1998; Keyhani and Rose- man, 1999), but relatively little is known about those Chitin is a linear polymer consisting of β-1, 4-linked isolated from freshwater. N-acetyl-D-glucosamine residues. It occurs in the exo- We have been studying chitinolytic bacteria living in skeletons of insects, mollusks, and crustaceans as freshwater such as lakes, rivers, and moats to clarify well as in the cell walls of many fungi. In nature, more their role in the recycling of chitin-related compounds than 1011 metric tons of chitin is synthesized each year in freshwater. We already isolated the chitinolytic bac- in the aquatic biosphere alone, and a corresponding terium Aeromonas hydrophila strain SUWA-9 from amount is degraded during the same period of time Lake Suwa, a freshwater lake located in Nagano Pre- (Yu et al., 1993). A large number of chitinolytic bacteria fecture, Japan (Lan et al., 2004). We reported that the have been isolated from soil and seawater and their strain produced several kinds of endo- and exo-type chitin-degrading enzymes have been characterized chitinolytic enzymes in the presence of the substrate, chitin (Lan et al., 2006, 2008). During the screening of chitinolytic bacteria from * Address reprint requests to: Dr. Makoto Shimosaka, Divi- moat water of Ueda Castle in Nagano Prefecture, Ja- sion of Applied Biology, Faculty of Textile Science and Technol- pan, we isolated a bacterial strain that grew well on ogy, Shinshu University, 3‒15‒1 Tokida, Ueda, Nagano 386‒8567, Japan. synthetic medium containing colloidal chitin as a sole Tel and Fax: +81‒268‒21‒5341 carbon source. A phylogenetic analysis based on 16S E-mail: [email protected] rRNA gene sequences showed that this bacterial strain 148 SATO et al. Vol. 55 named SAY3T belongs to the family Neisseriaceae, but ODS 5C18 columns (4.6 × 150 mm). does not form a significant cluster with any species of Cellular fatty acid analysis. Cellular fatty acids were the known genera of this family. In this paper, we re- prepared according to the protocol of MIDI system. port the taxonomic characteristics of the strain and Cells were grown on TSBA medium at 30°C for 48 h. propose to classify it under a new genus and species The fatty acids were analyzed by gas chromatography with the name Chitiniphilus shinanonensis. controlled by MIS software (Microbial ID, Inc.). The peaks were integrated and identified by the Microbial Materials and Methods Identification software package (Sasser, 1990). Determination of G+C content. Genomic DNA was Isolation of bacterial strains. The bacterial strain prepared according to the method of Sambrook et al. SAY3T used in this study was isolated from moat water (1989). Total DNA was digested with P1 nuclease us- of Ueda Castle in Nagano Prefecture, Japan. A nylon ing a Yamasa GC kit (Yamasa Shoyu Co., Chiba, Ja- bag containing chitin flakes (a gift from Kyowa Tech- pan). The G+C content of DNA was determined by nos Co., Ltd., Japan) was soaked in moat water for HPLC method as described by Mesbah et al. (1989). 14 days, and then the chitin flakes were recovered and 16S rRNA gene sequencing and phylogenetic analy- washed with tap water. Then the 0.2 g of chitin flakes sis. Chromosomal DNA was isolated from the cells were inoculated into 100 ml of synthetic medium (0.5% and purified by InstaGene Matrix kit (Bio-Rad Labora- (NH4)2SO4, 0.085% KH2PO4, 0.015% K2HPO4, 0.05% tories, CA, USA). PCR was performed with PrimeSTAR MgSO4, 0.01% NaCl, 0.01% CaCl2) containing 0.2% HS DNA Polymerase (TaKaRa Bio, Inc., Shiga, Japan) powder chitin (from crab shells, Nacalai Tesque, Ja- with sets of primers encompassing a whole 16S rRNA pan) as the sole carbon source. The flask was shaken gene. Sequencing was conducted with the BigDye vigorously at 25°C until the culture showed a signifi- Terminator v3.1 Cycle Sequencing Kit (Applied Biosys- cant turbidity caused by cell growth. Then a portion of tems, Inc., CA, USA) using the ABI PRISM 3100 Ge- the culture was transferred into a fresh medium of the netic Analyzer System (Applied Biosystems, Inc.). The same composition. This inoculation step was repeated 16S rRNA gene sequence of the new isolate was de- several times to enrich chitin-degrading bacteria. Fi- termined and compared to those of related taxa re- nally chitin-degrading bacterial strains were isolated trieved from the DDBJ/GenBank/EMBL databases. For and purified on synthetic agar medium containing col- the multiple alignments, ClustalX2 program (Thomp- loidal chitin as the sole carbon source. son et al., 1997) was used. Alignment positions with Characterization of morphology, biochemistry, and gaps and unidentified bases were excluded with the phenotypes. Cell morphology was determined with a BioEdit program (Hall, 1999). The phylogenetic tree in light microscope (Olympus BX50F4, Tokyo, Japan). the neighbor-joining method (Saitou and Nei, 1987) Flagellation was observed using a transmission elec- was constructed using the Neighbor program in tron microscope (JEM-100 SX, JEOL, Ltd., Tokyo, Ja- PHYLIP (PHYLogeny Inference Package). Branching pan) after negative-staining with phosphotungstic patterns of the tree were evaluated by bootstrapping acid. Utilization of carbon sources and some enzyme with 1,000 resamplings, and the evolutionary distance activities were determined using API20NE, API 50CH was computed using the Kimura’s 2-parameter model and API ZYM (bioMerieux, Paris, France). Oxidase ac- (Kimura, 1980). The tree was illustrated using the Tree- tivity was determined by oxidation of 1% tetramethyl-p- Explorer program (Kumar et al., 2001). Maximum-like- phenylenediamine. Catalase activity was determined lihood tree was constructed using the Dnaml program by bubble production in 3% (v/v) H2O2. in PHYLIP. Respiratory quinone analysis. Isoprenoid quinones were extracted from freeze-dried cells with chloroform： Results methanol (2：1, v/v), and fractionated with thin-layer chromatography developed with n-hexane：diethyl Isolation of the bacterial strain ether (85：15, v/v). Quinones were detected under UV The chitinolytic bacterial strain was isolated from light at 275 nm. The ubiquinone fraction was extracted moat water by collecting bacterial cells tightly bound with acetone, dried under a nitrogen gas stream, and on the surface of chitin flakes. After enrichment of cells analyzed by HPLC (Shimadzu LC-10A) with a Nacalai grown in synthetic medium containing chitin powder 2009 Chitiniphilus shinanonensis gen. nov., sp. nov. 149 as the sole carbon source, one strain growing well and Table 1. Utilization of carbon compounds by the strain SAY3T. producing a clear halo around the colony was isolated Carbon compounds Result on synthetic agar medium containing colloidal chitin. Preliminary study on the partial sequence of 16S rRNA Glycerol - gene revealed that it did not show identity (more than Erythritol - D-Arabinose - 97%) to the sequences of the known bacteria available L-Arabinose - T in the public database. This strain named SAY3 was D-Ribose + further investigated for its taxonomic characteristics. D-Xylose - L-Xylose - Morphological and physiological characteristics D-Adonitol - β Strain SAY3T is a gram-negative, non-spore-forming Methyl- -D-xylopyranoside - D-Galactose - and curved rod-shaped cell of 0.7‒0.8 μm in width and D-Glucose + 1.2 1.5 μm in length. The strain formed circular, smooth, ‒ D-Fructose +w pale yellow colonies with rhizoid margins when it grew D-Mannose + on LB agar plate at 30°C for 48 h. Cells were motile L-Sorbose - with single polar flagellum (Fig. 1). The strain was a L-Rhamnose - facultative anaerobic and grew at 15‒45°C (optimum Dulcitol - Inositol 30‒37°C) but did not grow at 10°C. It did not grow in - D-Mannitol - the presence of 4% NaCl. D-Sorbitol - Utilization of carbon sources and some enzyme ac- Methyl-α-D-mannopyranoside - tivities were determined using API 20NE, API 50CH Methyl-α-D-glucopyranoside - and API ZYM (Tables 1, 2 and 3). The strain utilized a N-Acetyl-glucosamine + narrow range of carbon sources, such as D-glucose, Amygdalin + D-mannose, N-acetyl-D-glucosamine, D-ribose, amyg- Arbutin - Esculin ferric citrate + dalin, esculin ferric citrate, and salicin.
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