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Physiological and Genomic Features of a Novel Violacein-Producing Bacterium Isolated from Surface Seawater

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Physiological and Genomic Features of a Novel Violacein-Producing Bacterium Isolated from Surface Seawater RESEARCH ARTICLE Physiological and genomic features of a novel violacein-producing bacterium isolated from surface seawater Yue-Hong Wu, Hong Cheng, Lin Xu, Xiong-Bin Jin, Chun-Sheng Wang, Xue-Wei Xu* Key Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou, P. R. China * [email protected] a1111111111 a1111111111 Abstract a1111111111 a1111111111 Strains JW1T and JW3, isolated from surface seawater of the Arabian Sea, were subjected a1111111111 to polyphasic taxonomic analysis. Cells of both strains were Gram-stain-negative, aerobic, and rod-shaped. They formed violet pigment and produced violacein. On the basis of 16S rRNA gene sequence analysis, strains JW1T and JW3 showed high 16S rRNA gene sequence similarity with Pseudoalteromonas byunsanensis JCM12483T (98.2%), P. shioya- OPEN ACCESS sakiensis SE3T (97.8%), P. arabiensis JCM 17292T (97.3%), and P. gelatinilytica NH153T Citation: Wu Y-H, Cheng H, Xu L, Jin X-B, Wang C- (97.1%). The 16S rRNA gene sequence similarity between JW1T and JW3 was 100%. Phy- S, Xu X-W (2017) Physiological and genomic logenetic analyses revealed that both strains fell within the cluster of the genus Pseudoalter- features of a novel violacein-producing bacterium isolated from surface seawater. PLoS ONE 12(6): omonas and represented an independent lineage. The average nucleotide identity and in T e0179997. https://doi.org/10.1371/journal. silico DNA-DNA hybridization values between JW1 and type strains of the closely related pone.0179997 Pseudoalteromonas species were 70.9±83.3% and 20.0±26.4%, respectively. The sole Editor: Beom Seok Kim, Korea University, respiratory quinone in both strains is ubiquinone 8 (Q-8). The principal fatty acids are REPUBLIC OF KOREA summed feature 3 (C16:1ω7c and/or iso-C15:0 2OH), C18:1ω7c, and C16:0. The major polar Received: January 15, 2017 lipids are phosphatidylethanolamine, phosphatidylglycerol, one unidentified glycolipid, one Accepted: June 7, 2017 unidentified aminolipid, and one unidentified phospholipid. The DNA G+C content was 43.3 mol%. Differential phylogenetic distinctiveness, chemotaxonomic differences, and pheno- Published: June 22, 2017 typic properties indicated that strains JW1T and JW3 could be differentiated from the Pseu- Copyright: © 2017 Wu et al. This is an open access doalteromonas species with validly published names. Therefore, it is proposed that strains article distributed under the terms of the Creative T Commons Attribution License, which permits JW1 and JW3 represent a novel species of the genus Pseudoalteromonas, for which the T T unrestricted use, distribution, and reproduction in name Pseudoalteromonas amylolytica sp. nov. (type strain, JW1 = CGMCC 1.15681 = any medium, provided the original author and KCTC 52406T = MCCC 1K02162T) is proposed. source are credited. Data Availability Statement: The GenBank/EMBL/ DDBJ accession numbers for the 16S rRNA gene sequence of strains JW1T and JW3 are KU535632 and KU535631. The GenBank accession numbers for the whole genome sequences of strains JW1T, Introduction JW3 and P. byunsanensis JCM12483T are The genus Pseudoalteromonas, the type genus of the family Pseudoalteromonadaceae [1], was MKJU00000000, MKJT00000000 and MNAN00000000, respectively. Other relevant data proposed by Gauthier et al. (1995) [2]. Initially, the genus Pseudoalteromonas was differenti- are within the paper and its Supporting Information ated from the genus Alteromonas based on the phylogenetic analysis of 16S rRNA gene files. sequences [2]. Currently, the genus Pseudoalteromonas consists of 43 species with validly PLOS ONE | https://doi.org/10.1371/journal.pone.0179997 June 22, 2017 1 / 14 Novel violacein producer isolated from surface seawater Funding: This work was supported by the National published names (http://www.bacterio.net/p/pseudoalteromonas.html). Members of the genus Natural Science Foundation of China granted to YW Pseudoalteromonas are widespread in nature and have a great adaptability to marine environ- (no. 41406174, http://www.nsfc.gov.cn/publish/ ments, such as coastal, open, and deep seawaters, sediments, marine invertebrates, fish, and portal1/); the National Key Basic Research Program of China granted to XX (2014CB441503, http:// algae [3]. The genus Pseudoalteromonas is Gram-negative, aerobic or facultatively anaerobic, + most.gov.cn/); the Natural Science Foundation of and rod-shaped, it requires Na ions for growth, usually does not denitrify, and possesses ubi- Zhejiang Province granted to XX (LR17D060001, quinone-8 (Q8) as major respiratory quinone [3]. http://www.zjnsf.gov.cn/). The funders had no role Some Pseudoalteromonas species produce a variety of primary and secondary metabolites, in study design, data collection and analysis, including antibiotics [2], exopolymers [4, 5], hydrolytic enzymes [6, 7], and pigments [2, 8]. decision to publish, or preparation of the Violacein is a natural indolocarbazole compound formed by condensation of two molecules of manuscript. tryptophan [9]. It is a potential pharmaceutical agent owing to its extensive biological proper- Competing interests: The authors have declared ties, such as antibacterial, antiviral, antioxidant, and antitumor activities [10]. Pseudoalteromo- that no competing interests exist. nas luteoviolacea has been reported to produce violacein [11]. Here, we present a polyphasic study describing two novel violacein-producing strains, both of which were isolated from sur- face water of the Arabian Sea. Materials and methods Organisms and culture conditions Strains JW1T and JW3 were isolated from the surface seawater collected from the Arabian Sea (E67Ê N24Ê). The seawater samples were stored at 4ÊC until use. Natural seawater agar (pH 7.2±7.4) supplemented with 0.05% peptone (w/v; BD, Sparks, MD, USA) and 0.01% yeast extract (w/v; BD) was used for isolation. The seawater samples were diluted using the standard ten-fold dilution plating technique and spread on natural seawater agar. After ten days of aero- bic incubation at 30ÊC, two violet colonies, designated as JW1T and JW3, were picked from different samples and purified by repeated restreaking. The purity was confirmed by the uni- formity of cell morphology. The reference strains P. byunsanensis JCM 12483T, P. shioyasa- kiensis JCM 18891T, and P. arabiensis JCM 17292T were obtained from the JCM (Japan Collection of Microorganisms). The reference strain P. gelatinilytica NH153T was available in our lab [12]. Unless otherwise stated, the two strains were routinely cultured in marine broth 2216 (MB; BD) or on marine agar 2216 (MA; BD) at 30ÊC and stored at ±80ÊC with 30% (v/v) glycerol. 16S rRNA gene and genome sequence determination The 16S rRNA gene was amplified and analyzed as described previously [13]. PCR products were cloned into the vector pMD 19-T (TaKaRa, Dalian, China) and then sequenced to deter- mine the almost-complete sequence of the 16S rRNA gene. High-quality genomic DNA was extracted with the AxyPrep™ Bacterial Genomic DNA Miniprep Kit (Axygen Scientific, Inc., Union City, CA, USA). The genomes of strains JW1T, JW3, and P. byunsanensis JCM 12483T were sequenced using the Solexa paired-end sequencing technology with the Illumina HiSeq 2000 platform (Anoroad Gene Technology Co. Ltd, Beijing, China). One paired-end library was constructed with 500-bp insert size. The sequencing generated approx. 1 Gb of clean data (approx. 500-fold genome coverage). De novo assembly of the reads was carried out using SOAPdenovo (version 2.0.1) [14]. Assembly k-mer was tested from 57 to 64 for seeking the optimal value, using the abyss-pe script. Assembly quality was estimated using MUMmer [15]. Completeness of the genome sequence was addressed using the bioinformatics tool CheckM (http://ecogenomics.github.io/CheckM/) [16]. The complete sequence of the 16S rRNA gene was annotated via the RNAmmer 1.2 Server [17] and was compared with related sequences of reference organisms using the EzTaxon-e service [18]. PLOS ONE | https://doi.org/10.1371/journal.pone.0179997 June 22, 2017 2 / 14 Novel violacein producer isolated from surface seawater Phylogenetic status Phylogenetic analysis was carried out using ARB (release 6.0.2) [19] and the All-Species Living Tree Project database (LTPs123, September 2015) [20]. The 16S rRNA gene sequences of strains JW1T and JW3 were aligned with SILVA Incremental Aligner (SINA, version 1.2.11) (http://www.arb-silva.de) [21]. The alignment sequences were imported into the LTPs data- base and implemented in ARB. On the basis of the obtained All-Species Living Tree and the EzTaxon-e results, 24 species were selected and sequence data were aligned with ClustalW [22]. Phylogenetic trees were reconstructed using the MEGA 5 program package [23], using Algicola sagamiensis B-10-31T as the outgroup, by neighbor-joining [24], maximum-parsi- mony [25], and maximum-likelihood methods [26]. Tree topology was evaluated by bootstrap analysis using 1000 resample datasets. Kimura two-parameter model [27] was used to calculate evolutionary distances and reconstruct phylogeny (neighbor-joining and maximum-likelihood methods). The genomes of 20 type strains of Pseudoalteromonas species were retrieved from the Gen- Bank database (S1 Fig). Six housekeeping genes, atpD (beta subunit for ATP synthase), gyrB (DNA gyrase beta subunit), mreB (rod shape-determining protein), recA (RNA recombinase alpha subunit), rpoD (RNA polymerase), and topA (DNA topoisomerase I) were used for mul- tilocus sequence analysis (MLSA).
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