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Description of Gramella Forsetii Sp. Nov., a Marine Flavobacteriaceae Isolated from North Sea Water, and Emended Description of Gramella Gaetbulicola Cho Et Al

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Description of Gramella Forsetii Sp. Nov., a Marine Flavobacteriaceae Isolated from North Sea Water, and Emended Description of Gramella Gaetbulicola Cho Et Al NOTE Panschin et al., Int J Syst Evol Microbiol 2017;67:697–703 DOI 10.1099/ijsem.0.001700 Description of Gramella forsetii sp. nov., a marine Flavobacteriaceae isolated from North Sea water, and emended description of Gramella gaetbulicola Cho et al. 2011 Irina Panschin,1† Mareike Becher,2† Susanne Verbarg,1 Cathrin Spröer,1 Manfred Rohde,3 Margarete Schüler,4 Rudolf I. Amann,2 Jens Harder,2 Brian J. Tindall1 and Richard L. Hahnke1,* Abstract Strain KT0803T was isolated from coastal eutrophic surface waters of Helgoland Roads near the island of Helgoland, North Sea, Germany. The taxonomic position of the strain, previously known as ‘Gramella forsetii’ KT0803, was investigated by using a polyphasic approach. The strain was Gram-stain-negative, chemo-organotrophic, heterotrophic, strictly aerobic, oxidase- and catalase-positive, rod-shaped, motile by gliding and had orange–yellow carotenoid pigments, but was negative for flexirubin-type pigments. It grew optimally at 22–25 C, at pH 7.5 and at a salinity between 2–3 %. Strain KT0803T hydrolysed the polysaccharides laminarin, alginate, pachyman and starch. The respiratory quinone was MK-6. Polar lipids comprised phosphatidylethanolamine, six unidentified lipids and two unidentified aminolipids. The predominant fatty acids were iso-C15 : 0, iso-C17 : 0 3-OH, C16 : 1!7c and iso-C17 : 1!7c, with smaller amounts of iso-C15 : 0 2-OH, C15 : 0, anteiso-C15 : 0 and C17 : 1!6c. The G+C content of the genomic DNA was 36.6 mol%. The 16S rRNA gene sequence identities were 98.6 % with Gramella echinicola DSM 19838T, 98.3 % with Gramella gaetbulicola DSM 23082T, 98.1 % with Gramella aestuariivivens BG- MY13T and Gramella aquimixticola HJM-19T, 98.0 % with Gramella lutea YJ019T, 97.9 % with Gramella. portivictoriae DSM 23547T and 96.9 % with Gramella marina KMM 6048T. The DNA–DNA relatedness values were <35 % between strain KT0803T and type strains with >98.2 % 16S rRNA gene sequence identity. Based on the chemotaxonomic, phenotypic and genomic characteristics, strain KT0803T has been assigned to the genus Gramella, as Gramella forsetii sp. nov. The type strain is KT0803T (=DSM 17595T=CGMCC 1.15422T). An emended description of Gramella gaetbulicolaCho et al. 2011 is also proposed. The genus Gramella, with the type species Gramella echini- on this sampling station is given in Gerdts et al. [14]. The cola, was proposed by Nedashkovskaya et al. [1] and com- strain was cultivated on agar plates with artificial seawater prises species that were isolated either from coastal surface after Schut et al. [15], supplemented with a mixture of amino T seawater (G. flava LMG 27360 [2] and G. planctonica C- acids, carbohydrates, alcohols and carboxylic acids at 25 C T CAMWZ-3 [3, 4]), from tidal flat sediment (G. portivictoriae [13]. In the aforementioned study, strain KT0803T was named T T UST040801-001 [5], G. gaetbulicola RA5-111 [6], G. aes- Cytophaga sp. KT0803 (NCBI taxon ID: 120668), but has T T tuarii BS12 [7], G. oceani CC-AMSZ-T [8], G. aestuarii- been studied for a long time as ‘Gramella forsetii’ (NCBI taxon vivens BG-MY13T [9] and G. aquimixticola MY13T [10], and T ID: 411154). Bauer et al. [16] showed, based on the genome of G. lutea YJ019 [11], or from sea urchins (G. echinicola KMM strain KT0803T, that this strain has a huge potential for sur- 6050T [1] and G. marina KMM 6048T [12]. face adhesion and hydrolyses glycosides and proteins using This study investigates the taxonomic position of strain glycoside hydrolases and peptidases, respectively. Further- KT0803T which was isolated by Eilers et al. [13] in August more, strain KT0803T lacks genes encoding for chitin degra- 1999 from coastal eutrophic surface waters (1 m depth) at the dation and for the assimilation of nitrate, nitrite and urea [16]. sampling station Helgoland Roads (54 09¢ N 7 52¢ E) near Using proteomics, three major polysaccharide utilization loci the island of Helgoland in the North Sea. More information [17] were detected in the genome of strain KT0803T enabling Author affiliations: 1Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany; 2Max Planck Institute for Marine Microbiology, Bremen, Germany; 3Helmholtz Centre for Infection Research, Braunschweig, Germany; 4Cell Biology and Electron Microscopy, University of Bayreuth, Bayreuth, Germany. *Correspondence: Richard L. Hahnke, [email protected] Keywords: North Sea; Flavobacteriaceae; polysaccharides; Helgoland. †These authors contributed equally to this work. The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain KT0803T is AF235117, and for the complete genome CU207366 Three supplementary figures and two supplementary tables are available with the online Supplementary Material. 001700 ã 2017 IUMS 697 Panschin et al., Int J Syst Evol Microbiol 2017;67:697–703 the strain to hydrolyse (i) a-1,4-glucans (e.g. glycogen, starch, Bacto Marine broth) supplemented with different azurin- amylose), (ii) laminarin-like polysaccharides and (iii) alginate- cross-linked (AZO-CL)-polysaccharides, casein and gelatin like polysaccharides [18]. Furthermore, most of the TonB- at 25 C for up to 14 days. Each 200 µl well of a microtitre dependent transporters, carbohydrate active enzymes and plate was filled with a small portion of one of the AZO-CL- SusD-like proteins that were involved in the decomposition of polysaccharides, AZO-CL-casein (Megazym), charcoal-pec- these polysaccharides were not secreted into the medium but tin, -gelatin (chapter 15.3.32.3, method 3; [23] and 100 µl were membrane-bound [18]. Gliding motility and identifica- medium. Each well was inoculated with 100 µl of a starved tion of the associated genes of strain KT0803T were docu- culture or 100 µl medium as control. Susceptibility to antibi- mented by McBride and Zhu [19] using liquid-filled tunnel otics was tested using the diffusion method with discs con- taining ampicillin (10 µg ml–1), erythromycin (15 µg ml–1), slides and modified Cytophaga agar (DSMZ medium 172). –1 –1 T rifampicin (5–30 µg ml ), streptomycin (10–50 µg ml ), Here we describe strain KT0803 in relation to previously –1 –1 published species of the genus Gramella using a polyphasic tetracycline (30 µg ml ) and vancomycin (30 µg ml ). taxonomy including phenotypic, chemotaxonomic and geno- Genomic DNA of strain KT0803T was isolated using the mic characteristics, 16S rRNA gene-based phylogeny, and Wizard Genomic DNA Purification Kit (Promega). Photo- DNA–DNA hybridization. metric DNA–DNA hybridization with strain KT0803T and Gramella gaetbulicola DSM 23082T were performed in Oxidase activity was tested using filter-paper discs (Sarto- duplicate as described by De Ley et al. [24] with the modifi- rius grade 388) impregnated with 1 % solution of N,N,N’, cations suggested by Huss et al. [25] using a Cary 100 Bio N’-tetramethyl-p-phenylenediamine (Sigma-Aldrich); the UV/visual spectrophotometer equipped with a Peltier- blue–purple colour after adding the cells indicated a posi- thermostat 6Â6 multicell changer and a temperature con- tive test. Catalase activity was tested by adding drops of 3 % troller with in situ temperature probe (Varian). Genomic H O to the cells; the observation of bubbles indicated a 2 2 DNA–DNA hybridizations (dDDH) were performed using positive test. The presence of flexirubin-type pigments was the Genome-to-Genome Distance Calculator (2.0), formula investigated according to the KOH test of Bernardet et al. 2 [26, 27]. The G+C content of the chromosomal DNA was [20]. Temperature optimum and pH optimum were determined in silico from the genome. Genes encoding car- determined on BD-Difco marine broth for temperatures bohydrate active enzymes and peptidases were retrieved from 0–42 C in steps of 2.5 C and pH values from 3.7–9.0 from the genome using the CAZy [28, 29] and MEROPS in increments of 0.5. Salinity optimum was determined in [30] databases, respectively. medium with salinities from 0–7 % by mixing 4Â marine broth solution (without NaCl, MgSO4 and CaCl2) with dif- For cellular fatty acid analysis, fatty acid methyl esters were ferent volumes of a 10Â saline solution (per litre: 194.5 g extracted from cells of strain KT0803Tcultivated on marine NaCl, 85.71 g MgCl2 6 H2O, 18 g CaCl2 2 H2O and MilliQ broth (DSMZ medium 514) at 25 C for 2 days. Cell samples water). Gliding motility was investigated by the hanging- were harvested by centrifugation at 3000 r.p.m., 20 C for drop method after Bernardet et al. [20] and by plating a 20 min during exponential growth phase. Fatty acid methyl droplet of a fresh culture on marine broth and HaHa soft esters were prepared and analysed using the protocol of agar (0.3 % agar, w/v). Utilization of carbon compounds K€ampfer and Kroppenstedt [31], followed by gas chroma- and acid production were determined using API 20 NE and tography (Agilent 5890). The microbial identification stan- API 50 CHE strips (bioMerieux) and GEN II MicroPlates dard software package MIDI Sherlock (version 6.1) [32] was (Biolog) according to the manufacturers’ instructions, with used to automatically integrate the peaks, annotate the fatty the following modifications. For API tests, the API medium acids and determine the relative percentages using TSBA40 (AUX, API 50 CHB/E) was either (i) mixed 1 : 1 with 2Â and TSBA50 databases. Respiratory lipoquinones were artificial seawater, 0.5 ml 0.3 % agar (Bacto, BD) and 0.1 % extracted from freeze-dried cell material with methanol/ (w/v, final) yeast extract (Oxoid), or (ii) supplemented with hexane, separated into their functional classes by thin-layer 3 % (v/v, final) seawater (Biomaris). The GEN II Micro- chromatography (TLC) and analysed by reverse-phase Plates were prepared with cells washed twice with HaHa HPLC as described by Tindall [33, 34].
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