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Diverse Cone-Snail Species Harbor Closely Related Streptomyces fmicb-08-02305 November 23, 2017 Time: 16:41 # 1 ORIGINAL RESEARCH published: 24 November 2017 doi: 10.3389/fmicb.2017.02305 Edited by: Jem Stach, Newcastle University, United Kingdom Diverse Cone-Snail Species Harbor Reviewed by: D. Ipek Kurtboke, Closely Related Streptomyces University of the Sunshine Coast, Australia Changsheng Zhang, Species with Conserved Chemical South China Sea Institute of Oceanology (CAS), China and Genetic Profiles, Including *Correspondence: Robert J. Capon Polycyclic Tetramic Acid [email protected] Francisco Barona-Gómez Macrolactams [email protected] 1†‡ 2†‡ 2† †Present address: Michelle Quezada , Cuauhtemoc Licona-Cassani , Pablo Cruz-Morales , Cuauhtemoc Licona-Cassani, Angela A. Salim1, Esteban Marcellin3, Robert J. Capon1* and Centro de Biotecnología FEMSA, Francisco Barona-Gómez2* Tecnológico de Monterrey, Monterrey, 1 2 Mexico Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia, Evolution of Metabolic Diversity 3 Michelle Quezada, Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, Mexico, Australian Institute for School of Environmental and Life Bioengineering and Nanotechnology, The University of Queensland, Brisbane, QLD, Australia Sciences, The University of Newcastle, Callaghan, NSW, Streptomyces are Gram-positive bacteria that occupy diverse ecological niches Australia Pablo Cruz-Morales, including host-associations with animals and plants. Members of this genus are known Australian Institute for Bioengineering for their overwhelming repertoire of natural products, which has been exploited for and Nanotechnology, The University of Queensland, Brisbane, QLD, almost a century as a source of medicines and agrochemicals. Notwithstanding intense Australia scientific and commercial interest in Streptomyces natural products, surprisingly little is ‡These authors have contributed known of the intra- and/or inter-species ecological roles played by these metabolites. In equally to this work. this report we describe the chemical structures, biological properties, and biosynthetic Specialty section: relationships between natural products produced by Streptomyces isolated from internal This article was submitted to tissues of predatory Conus snails, collected from the Great Barrier Reef, Australia. Using Antimicrobials, Resistance and Chemotherapy, chromatographic, spectroscopic and bioassays methodology, we demonstrate that a section of the journal Streptomyces isolated from five different Conus species produce identical chemical and Frontiers in Microbiology antifungal profiles – comprising a suite of polycyclic tetramic acid macrolactams (PTMs). Received: 01 April 2017 To investigate possible ecological (and evolutionary) relationships we used genome Accepted: 08 November 2017 Published: 24 November 2017 analyses to reveal a close taxonomic relationship with other sponge-derived and free- Citation: living PTM producing Streptomyces (i.e., Streptomyces albus). In-depth phylogenomic Quezada M, Licona-Cassani C, analysis of PTM biosynthetic gene clusters indicated PTM structure diversity was Cruz-Morales P, Salim AA, Marcellin E, Capon RJ and governed by a small repertoire of genetic elements, including discrete gene acquisition Barona-Gómez F (2017) Diverse events involving dehydrogenases. Overall, our study shows a Streptomyces-Conus Cone-Snail Species Harbor Closely ecological relationship that is concomitant with specific PTM chemical profiles. We Related Streptomyces Species with Conserved Chemical and Genetic provide an evolutionary framework to explain this relationship, driven by anti-fungal Profiles, Including Polycyclic Tetramic properties that protect Conus snails from fungal pathogens. Acid Macrolactams. Front. Microbiol. 8:2305. Keywords: Streptomyces, cone snails, natural product, phylogenomics, polycyclic tetramic acid macrolactams doi: 10.3389/fmicb.2017.02305 (PTMs) Frontiers in Microbiology| www.frontiersin.org 1 November 2017| Volume 8| Article 2305 fmicb-08-02305 November 23, 2017 Time: 16:41 # 2 Quezada et al. Evolutionary Reconstruction of PTM Biosynthesis INTRODUCTION Cone snails are marine molluscs that comprise the large genus Conus, with currently over 800 species identified (Costello et al., Polycyclic tetramic acid macrolactams (PTMs) are widespread 2013). Queensland, Australia, represents a biodiversity hotspot natural products produced by members of the phyla for these molluscs with 133 of 166 Australian species. Cone snails Actinobacteria and Proteobacteria (class gammaproteobacteria). prey on fish, worms or other snails using venoms composed PTM-producing bacteria have been isolated from complex mainly of small peptides (<5 kDa) known as conotoxins or biological systems, such as sponges, plants and insects (Shigemori conopeptides. Conotoxins are chemically stable ribosomally et al., 1992; Jakobi and Winkelmann, 1996; Nakayama et al., synthesized and post-translationally modified peptides that 1999; Yu et al., 2007; Blodgett et al., 2010). Examples of possess high specificity against diverse neuronal targets, many PTMs produced by symbiotic bacteria include alteramide A of which are implicated in human diseases (Cruz et al., produced by Alteromonas sp., isolated from the marine sponge 1985; Vetter and Lewis, 2012; Inserra et al., 2013). Given Halichondria okadai (Shigemori et al., 1992), maltophilin the wide range of potential applications of conotoxins as produced by Stenotrophomonas maltophilia, isolated from the pharmaceutics, cone snails have proved to be an excellent rhizosphere of rape plants (Jakobi and Winkelmann, 1996), source of molecules for drug discovery and development (Adams xanthobaccins produced by Stenotrophomonas sp. strain SB-K88, et al., 1999; Halai and Craik, 2009). An example of this isolated from the root of sugar beet (Nakayama et al., 1999), is the conopeptide marketed under the name Prialt, used and frontalamides produced by Streptomyces sp. SPB78, isolated clinically as a pain therapeutic (Miljanich, 2004). Previous studies from the southern pine beetle (Blodgett et al., 2010). These on cone snail-associated bacteria as producers of bioactive observations suggest that PTMs play important biological and metabolites reported neuroactive metabolites (Lin et al., 2011, ecological roles yet-to-be described. 2013). Structurally, PTMs are composed of a polycyclic carbocycle In the current study, we explored the biosynthetic repertoire (5-5, 5-5-6 or 5-6-5 ring system), a macrolactam core, and a of five cone snail-derived Streptomyces isolated from cone snail tetramic acid moiety (Zhang et al., 2016). Functional analysis specimens collected from the Lady Musgrave Island, Great using the host Escherichia coli for heterologous expression, Barrier Reef, Australia. The observation that several Streptomyces and in vitro reconstitution of individual functional polyketide isolates displayed common phenotypic colony morphology when (PKS) and non-ribosomal synthetase (NRPS) enzymes, have grown under specific culture conditions, suggested a taxonomic determined that the tetramate polyene precursor is produced bias, and perhaps a common (ecological-symbiotic) relationship. via a hybrid PKS/NRPS, whereas the PKS domain is responsible This prompted us to conduct a chemical and phylogenomic for the PTM backbone assembly (Li et al., 2014) and the investigation, in which we confirmed that all isolates were NRPS module incorporates L-ornithine (Blodgett et al., 2010). taxonomically related, and shared similar chemical and biological In addition, the biosynthetic pathways of several PTMs (i.e., (i.e., antifungal) profiles. A phylogenomic approach was used frontalamides, ikarugamycin, and dihyrodromaltophilin – also to establish direct correlations between sequence phylogeny, known as heat-stable antifungal factor HSAF) have been the presence/absence of enzymes within the PTM BGCs, elucidated using different in vivo and in vitro approaches and the associated natural products. Overall, this report (Yu et al., 2007; Halo et al., 2008; Blodgett et al., 2010; demonstrates a specific association between a discrete lineage Lou et al., 2011; Antosch et al., 2014; Li et al., 2014; Zhang of Streptomyces and cone snails, and provides an evolutionary et al., 2014; Greunke et al., 2017). For instance, the six- framework for further investigations into the biosynthesis gene (ftdA-F) frontalamide biosynthetic gene cluster (BGC), of PTMs. identified by gene knock out of the ftd biosynthetic cluster in Streptomyces sp. SPB78, incorporates a sterol desaturase- like enzyme, iterative hybrid PKS/NRPS, two desaturase-like MATERIALS AND METHODS enzymes, a zinc dependent alcohol desaturase and a cytochrome P450 enzyme (Blodgett et al., 2010). The biosynthesis of Cone Snail Collection, Dissection and ikarugamycin from Streptomyces sp. was elaborated through Microbial Isolation heterologous expression of three main biosynthetic components, Cone snails and microorganisms were manipulated under sterile the iterative hybrid PKS/NRPS enzyme, phytoene desaturase- conditions provided by a LabTech class II biological safety cabinet like enzyme and alcohol dehydrogenase encoded by ikaA, ikaB, and incubated in either a MMM Friocell incubators (Lomb and ikaC genes, respectively (Antosch et al., 2014; Zhang Scientific, NSW, Australia) or an Innova 42R incubator shaker et al., 2014; Greunke et al., 2017). Finally, dihydromaltophilin (John Morris, NSW, Australia) with temperature set at 26.5◦C. biosynthesis was described in Lysobacter enzymogenes
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