Analysis of the genomic sequences and metabolites of Serratia surfactantfaciens sp. nov. YD25 T that simultaneously produces prodigiosin and serrawettin W2

Su et al. BMC Genomics (2016) 17:865 DOI 10.1186/s12864-016-3171-7 RESEARCH ARTICLE Open Access Analysis of the genomic sequences and metabolites of Serratia surfactantfaciens sp. nov. YD25T that simultaneously produces prodigiosin and serrawettin W2 Chun Su1, Zhaoju Xiang1, Yibo Liu1, Xinqing Zhao2, Yan Sun1*, Zhi Li1*, Lijun Li3, Fan Chang1, Tianjun Chen1, Xinrong Wen1, Yidan Zhou1 and Furong Zhao1 Abstract Background: Gram-negative bacteria of the genus Serratia are potential producers of many useful secondary metabolites, such as prodigiosin and serrawettins, which have potential applications in environmental bioremediation or in the pharmaceutical industry. Several Serratia strains produce prodigiosin and serrawettin W1 as the main bioactive compounds, and the biosynthetic pathways are co-regulated by quorum sensing (QS). In contrast, the Serratia strain, which can simultaneously produce prodigiosin and serrawettin W2, has not been reported. This study focused on analyzing the genomic sequence of Serratia sp. strain YD25T isolated from rhizosphere soil under continuously planted burley tobacco collected from Yongding, Fujian province, China, which is unique in producing both prodigiosin and serrawettin W2. Results: A hybrid polyketide synthases (PKS)-non-ribosomal peptide synthetases (NRPS) gene cluster putatively involved in biosynthesis of antimicrobial serrawettin W2 was identified in the genome of YD25T, and its biosynthesis pathway was proposed. We found potent antimicrobial activity of serrawettin W2 purified from YD25T against various pathogenic bacteria and fungi as well as antitumor activity against Hela cells. Subsequently, comparative genomic analyses were performed among a total of 133 Serratia species. The prodigiosin biosynthesis gene cluster in YD25T belongs to the type I pig cluster, which is the main form of pig-encoding genes existing in most of the pigmented Serratia species. In addition, a complete autoinducer-2 (AI-2) system (including luxS, lsrBACDEF, lsrGK, and lsrR) as a conserved bacterial operator is found in the genome of Serratia sp. strain YD25T. Phylogenetic analysis based on concatenated Lsr and LuxS proteins revealed that YD25T formed an independent branch and was clearly distant from the strains that solely produce either prodigiosin or serrawettin W2. The Fe (III) ion reduction assay confirmed that strain YD25T could produce an AI-2 signal molecule. Phylogenetic analysis using the genomic sequence of YD25T combined with phylogenetic and phenotypic analyses support this strain as a member of a novel and previously uncharacterized Serratia species. Conclusion: Genomic sequence and metabolite analysis of Serratia surfactantfaciens YD25T indicate that this strain can be further explored for the production of useful metabolites. Unveiling the genomic sequence of S. surfactantfaciens YD25T benefits the usage of this unique strain as a model system for studying the biosynthesis regulation of both prodigiosin and serrawettin W2 by the QS system. Keywords: Serratia, Antimicrobial activity, Genome comparisons, Serrawettin W2, Non-ribosomal peptide synthetases, Quorum sensing, Polyphasic taxonomy * Correspondence: ; 1 College of Life Sciences, Shaanxi Normal University, Xi’an 710119, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2016 Open Access 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. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Su et al. BMC Genomics (2016) 17:865 Background Gram-negative bacteria of the genus Serratia have been isolated from water, air, soil, plants, and animals and are members of the Enterobacteriaceae [1]. The ubiquity of Serratia is largely attributed to the variety of compounds that are released into the environment [2, 3]. Some species of Serratia such as S. plymuthica, S. rubidaea, S. marcescens and S. nematodiphila produce a nondiffusible red pigment identified as prodigiosin, which is an alkaloid secondary metabolite with a unique tripyrrole chemical structure [4]. In addition, some species of Serratia also produce various useful secondary metabolites including oocydin A, carbapenem, althiomycin, bacteriocins, and serrawettins [5–7]. These useful secondary metabolites have potential applications in the environmental bioremediation and pharmaceutical industry. Prodigiosin has been shown to have antimicrobial (antifungal, antibacterial, antiprotozoal), antimalarial, antitumor, and immunosuppressant activities at nontoxic levels [8–10]. Other important secondary metabolites are serrawettins, which are useful biosurfactants produced by Serratia [11]. Three molecular species, serrawettin W1, W2, and W3, have been reported [12]. Serrawettin W1 is a symmetric dilactone structure composed of two serine residues connected with two 3hydroxydecanoic acids [13]. It has been regarded as a good anti-cancer drug, which could inhibit cell growth and induce apoptosis of several cell lines derived from T-cell leukemia or Burkitt lymphoma [14, 15]. Serrawettin W2 contains a fatty acid connected with five amino acid residues, which was first isolated from S. marcescens in 1986 [16]. Serrawettin W2 is a biosurfactant that can disperse Caenorhabditis elegans [17], and antimicrobial activity against Staphylococcus aureus has been reported [18]. Moreover, there are fewer reports about the bioactivity of cyclic lipopeptides serrawettin W2 and W3. It was found that several Serratia strains, including S. marcescens ATCC 274 [19], S. marcescens 2170 [20], S. marcescens CH-1 [21], and S. marcescens NS-38 [12], could produce prodigiosin and serrawettin W1 at the same time. However, the strains that could parallel-produce prodigiosin and serrawettin W2 as the main bioactive compounds have not previously been published. Many active metabolites produced by Serratia strains are regulated by quorum sensing (QS), including butanediol fermentation; production of exoenzymes; nuclease and secondary metabolites such as biosurfactant, carbapenem, oocydin A; and prodigiosin [22–26]. Furthermore, a wide spectrum of important processes, such as bioluminescence, motility, sporulation, virulence, and biofilm formation, are also regulated by the QS system, which influences bacteria community gene regulation by cell–cell communication via the production and detection of diffusible auto-inducer Page 2 of 19 signaling molecules [27]. Generally, the most extensively described QS system in Gram-negative ba (...truncated)