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Halomonas Smyrnensis AAD6T Elif Diken1, Tugba Ozer1, Muzaffer Arikan2, Zeliha Emrence2, Ebru Toksoy Oner1, Duran Ustek3 and Kazim Yalcin Arga1*

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Halomonas Smyrnensis AAD6T Elif Diken1, Tugba Ozer1, Muzaffer Arikan2, Zeliha Emrence2, Ebru Toksoy Oner1, Duran Ustek3 and Kazim Yalcin Arga1* Diken et al. SpringerPlus (2015) 4:393 DOI 10.1186/s40064-015-1184-3 RESEARCH Open Access Genomic analysis reveals the biotechnological and industrial potential of levan producing halophilic extremophile, Halomonas smyrnensis AAD6T Elif Diken1, Tugba Ozer1, Muzaffer Arikan2, Zeliha Emrence2, Ebru Toksoy Oner1, Duran Ustek3 and Kazim Yalcin Arga1* Abstract Halomonas smyrnensis AAD6T is a gram negative, aerobic, and moderately halophilic bacterium, and is known to pro- duce high levels of levan with many potential uses in foods, feeds, cosmetics, pharmaceutical and chemical industries due to its outstanding properties. Here, the whole-genome analysis was performed to gain more insight about the biological mechanisms, and the whole-genome organization of the bacterium. Industrially crucial genes, including the levansucrase, were detected and the genome-scale metabolic model of H. smyrnensis AAD6T was reconstructed. The bacterium was found to have many potential applications in biotechnology not only being a levan producer, but also because of its capacity to produce Pel exopolysaccharide, polyhydroxyalkanoates, and osmoprotectants. The genomic information presented here will not only provide additional information to enhance our understanding of the genetic and metabolic network of halophilic bacteria, but also accelerate the research on systematical design of engineering strategies for biotechnology applications. Keywords: Halomonas smyrnensis, Halophiles, Genome, Next-generation sequencing, Levan Background of levan, which is a long linear homopolymeric EPS of Halomonas smyrnensis AAD6T is a rod-shaped, Gram- ß(2-6)-linked fructose residues (Poli et al. 2009). Levan negative, aerobic, exopolysaccharide (EPS) producing and has been credited as one of the most promising polysac- moderately halophilic bacterium, growing at salt con- charides for foods, feeds, cosmetics, pharmaceutical and centration in the range of 3–25% (w/v) NaCl (optimum, chemical industries (Donot et al. 2012) and, potential 10%), at temperatures between 5 and 40°C (optimum, uses of levan produced by AAD6T, as a bioactive poly- 37°C), and pH values between 5.5 and 8.5 (optimum, mer, were reported (Costa et al. 2013; Kucukasik et al. 7.0) (Poli et al. 2012). The strain utilizes glucose, sucrose, 2011; Sam et al. 2011; Sezer et al. 2011; Sima et al. 2011, maltose, arabinose, raffinose, fructose, galactose, and 2012). mannose as a sole carbon and energy source, and alanine When compared to the other groups of extremophilic and serine as a sole carbon, nitrogen and energy source microorganisms such as the thermophiles, the halophiles (Poli et al. 2009, 2012). The EPS production by H. smyrn- have been relatively little exploited in biotechnological ensis AAD6T is growth-associated, and when sucrose processes with a few exceptions (Pastor et al. 2010; Philip was used as carbon source the bacteria excrete high levels et al. 2007; Rodriguez-Valera and Lillo 1992; Sam et al. 2011). On the other hand, due to their osmoadaptation abilities and metabolic capabilities for the production *Correspondence: [email protected] 1 Department of Bioengineering, Marmara University, Goztepe, of compatible solutes, bioplastics, nutritional products, 34722 Istanbul, Turkey biopolymers, and halophilic enzymes, they represent Full list of author information is available at the end of the article considerable potential in various industries including © 2015 Diken et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Diken et al. SpringerPlus (2015) 4:393 Page 2 of 11 chemical, environmental, biofuel, medical, pharmaceuti- optimum semi-chemical medium (Poli et al. 2009) was cal and health care. used in growth cultures. To obtain the highest growth In systems biology research, the microbial genome rate without EPS production, glucose was added as sole sequence is the starting point for detailed analysis of carbon source to chemical medium at concentration of identifying gene-protein associations and metabolic 10 g/L. reconstruction. In this context, next generation sequenc- The genome of H. smyrnensis AAD6T was sequenced ing (NGS) technologies play an important role since by the whole genome shotgun approach using a combina- they provide high-throughput genomic data, includ- tion of 454 GS FLX+ (454 Life Sciences, Branford, CT) ing whole genome sequences (WGS), at unprecedented and Ion Torrent (Ion Torrent Systems, Inc., Guilford, CT) speed with relatively low cost (Gov and Arga 2014; Zhang sequencers and the generated shotgun sequence data was et al. 2011). WGS data provide many advantages in com- assembled as described in (Sogutcu et al. 2012). parative genomics and metabolic engineering. In addi- tion to the nucleotide sequence and protein sequences Genome annotation of the encoded proteins, the gene content, the order of Gene prediction and genome annotation were carried out genes and the predicted enzymes on the genome may using the RAST auto-annotation server (Aziz et al. 2008). be informative for phylogenetic analyses and metabolic Protein-encoding and transfer RNA genes were predicted reconstructions. Moreover, WGS information facilitates by RAST server, while the ribosomal RNA genes were the acquirement of functional genomics data. identified with RNAmmer (v1.2) (Lagesen et al. 2007). To design economical production schemes, fermenta- The gene predictions of essential biosystems were manu- tion conditions and effective stimulatory factors for levan ally verified using BLAST searches against protein data- production by H. smyrnensis AAD6T was analyzed sys- bases, the Universal Protein Resource (UniProt) (http:// tematically (Ateş et al. 2013; Ates et al. 2011; Sarilmiser www.uniprot.org/) and National Center for Biotechnol- Kazak et al. 2014). However, towards the design of effi- ogy Information (NCBI) (http://www.ncbi.nlm.nih.gov/). cient microbial cell factories for levan overproduction, The gene functions and classifications were based on the main bottleneck was the lack of information on the the subsystem annotation of the RAST server. Informa- genome of the microorganism. Considering this fact, tion on enzyme-encoding genes was taken from Kyoto we employed two different NGS technologies, namely, Encyclopedia of Genes and Genomes (KEGG) (Kanehisa Roche 454 GS FLX+ System and Ion Torrent Sequencer, et al. 2012) and ExPaSy databases (Artimo et al. 2012). and a hybrid NGS approach to develop a high-quality Transport protein coding genes were annotated using WGS data for H. smyrnensis AAD6T (Sogutcu et al. the similarity searches against the Transfer Classification 2012). Within the context of this study, the genome of Database (TCDB) (Saier et al. 2009). AAD6T was further analyzed to reveal the essential bio- logical mechanisms and the whole genomic organiza- Phylogenetic and phylogenomic analyses tion of levan producing H. smyrnensis AAD6T, and the The phylogenetic analyses were performed using PhyML genome-scale metabolic model of H. smyrnensis AAD6T (v3.0) and phylogenetic trees were reconstructed using was reconstructed. This understanding is crucial for maximum likelihood method (Guindon et al. 2010). The rational design and optimization of engineering strate- phylogenetic classification of bacterial strains was based gies for levan overproduction. Furthermore, the infor- on complete 16S rRNA sequences. The phylogenetic clas- mation provided here will facilitate future studies on the sification of a set of bacterial levansucrase enzymes was genetic and metabolic diversity of halophilic bacteria and based on nucleotide sequences taken from NCBI data- contribute to the employment of H. smyrnensis AAD6 in base. The phylogenomic comparison within the Halo- biotechnological processes. monadaceae family was based on the encoded proteins with putative functions assigned by the RAST server. Methods Encoded proteins were sorted out for all genomes and Bacterial strain comparatively analyzed based on the presence/absence of Halophilic bacterial strain H. smyrnensis AAD6T (JCM proteins. 15723, DSM 21644) used in this study was isolated from Çamaltı Saltern Area in Turkey (Poli et al. 2012). Reconstruction of the genome‑scale metabolic model The entire reconstruction procedure consists of an auto- Sequencing and assembly mated procedure followed by manual curation at the gap The genomic DNA was isolated from exponential-phase filing step. The preliminary model was built automatically cultures using the quick protocol of Wizard® Genomic via the Model SEED (Henry et al. 2010). The refinement DNA Purification Kit (Promega, Madison, WI). The of the model (for stand-alone reactions or metabolites, Diken et al. SpringerPlus (2015) 4:393 Page 3 of 11 and missing connections in essential metabolic pro- respectively). Most of the osmotic stress genes of H. cesses) was achieved via a non-automated but iterative smyrnensis AAD6T (47 coding sequences) encode pro- decision-making process, as described in (Ates et al. teins associated with choline and glycine betaine uptake, 2011). and glycine betaine biosynthesis pathways, which are involved in osmoprotection. Results and discussion At a large-scale comparison, the size of the genome, Sequencing
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