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Genomic Insights Into the Evolution of Hybrid Isoprenoid Biosynthetic Gene Clusters in the MAR4 Marine Streptomycete Clade

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Genomic Insights Into the Evolution of Hybrid Isoprenoid Biosynthetic Gene Clusters in the MAR4 Marine Streptomycete Clade UC San Diego UC San Diego Previously Published Works Title Genomic insights into the evolution of hybrid isoprenoid biosynthetic gene clusters in the MAR4 marine streptomycete clade. Permalink https://escholarship.org/uc/item/9944f7t4 Journal BMC genomics, 16(1) ISSN 1471-2164 Authors Gallagher, Kelley A Jensen, Paul R Publication Date 2015-11-17 DOI 10.1186/s12864-015-2110-3 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Gallagher and Jensen BMC Genomics (2015) 16:960 DOI 10.1186/s12864-015-2110-3 RESEARCH ARTICLE Open Access Genomic insights into the evolution of hybrid isoprenoid biosynthetic gene clusters in the MAR4 marine streptomycete clade Kelley A. Gallagher and Paul R. Jensen* Abstract Background: Considerable advances have been made in our understanding of the molecular genetics of secondary metabolite biosynthesis. Coupled with increased access to genome sequence data, new insight can be gained into the diversity and distributions of secondary metabolite biosynthetic gene clusters and the evolutionary processes that generate them. Here we examine the distribution of gene clusters predicted to encode the biosynthesis of a structurally diverse class of molecules called hybrid isoprenoids (HIs) in the genus Streptomyces. These compounds are derived from a mixed biosynthetic origin that is characterized by the incorporation of a terpene moiety onto a variety of chemical scaffolds and include many potent antibiotic and cytotoxic agents. Results: One hundred and twenty Streptomyces genomes were searched for HI biosynthetic gene clusters using ABBA prenyltransferases (PTases) as queries. These enzymes are responsible for a key step in HI biosynthesis. The strains included 12 that belong to the ‘MAR4’ clade, a largely marine-derived lineage linked to the production of diverse HI secondary metabolites. We found ABBA PTase homologs in all of the MAR4 genomes, which averaged five copies per strain, compared with 21 % of the non-MAR4 genomes, which averaged one copy per strain. Phylogenetic analyses suggest that MAR4 PTase diversity has arisen by a combination of horizontal gene transfer and gene duplication. Furthermore, there is evidence that HI gene cluster diversity is generated by the horizontal exchange of orthologous PTases among clusters. Many putative HI gene clusters have not been linked to their secondary metabolic products, suggesting that MAR4 strains will yield additional new compounds in this structure class. Finally, we confirm that the mevalonate pathway is not always present in genomes that contain HI gene clusters and thus is not a reliable query for identifying strains with the potential to produce HI secondary metabolites. Conclusions: We found that marine-derived MAR4 streptomycetes possess a relatively high genetic potential for HI biosynthesis. The combination of horizontal gene transfer, duplication, and rearrangement indicate that complex evolutionary processes account for the high level of HI gene cluster diversity in these bacteria, the products of which may provide a yet to be defined adaptation to the marine environment. Keywords: Biosynthetic gene clusters, Genome evolution, Streptomyces, ABBA prenyltransferases, Secondary metabolism, Hybrid isoprenoids * Correspondence: [email protected] Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0204, USA © 2015 Gallagher and Jensen. 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. Gallagher and Jensen BMC Genomics (2015) 16:960 Page 2 of 13 Background molecules and thus play a critical role in the biosynthesis In bacteria, the genes responsible for the biosynthesis of of HI secondary metabolites. These enzymes also play secondary metabolites are typically clustered on the important roles in the biosynthesis of primary metabo- chromosome [1]. These biosynthetic gene clusters evolve lites including membrane sterols and lipoquinones [19]. rapidly relative to other genetic elements [2, 3], which One sub-group of PTases specific to secondary metabol- likely contributes to the remarkable structural diversity ism are the ABBA PTases, named in reference to the observed among secondary metabolites. While the se- ααββ structural repeats that form a large β-barrel fold lective pressures driving secondary metabolite diversifi- comprising the active center of the enzyme. ABBA cation remain largely unknown, the availability of large PTases attach isoprene moieties to aromatic substrates numbers of genome sequences has made it possible to and, to date, all characterized ABBA PTases are involved begin to identify the evolutionary mechanisms that gov- in the biosynthesis of HI secondary metabolites [20]. ern the biogenesis of structural novelty [2–4]. ABBA PTases can be further divided into two sub- The genus Streptomyces is well known as the source of groups, both of which are found in fungi and bacteria. structurally diverse secondary metabolites [5, 6]. With The first group is the indole ABBA PTases, which are re- nearly 600 named species, it is the most specious of all sponsible for the prenylation of indole substrates. One bacterial genera and comprises the majority of diversity example is the enzyme CymD, which is responsible for within the family Streptomycetaceae. Streptomycetes are prenylation of the bacterial cyclic peptide cyclomarin typically saprophytic and found in terrestrial soils and [21]. The second group is the ‘Orf2’ PTases, which marine sediments. They also occur as plant endophytes, attach isoprenoid moieties to a variety of aromatic invertebrate mutualists, and human or plant pathogens substrates including phenazines, naphthoquinones, and [7, 8]. Within the genus Streptomyces, the ‘MAR4’ clade aminocoumarins. This group is named for the first has been described as a largely marine-derived lineage characterized member, later renamed ‘NphB’, which is in- [9]. Based on available sequence data, it currently en- volved in naphterpin biosynthesis [22]. Although the in- compasses 57 cultured strains and 180 cloned sequences dole and Orf2 PTases bear little sequence homology, and displays 4.1 % 16S rRNA divergence. Members of they are thought to have arisen from a common ancestor this clade consistently form two sub-clades represented [20]. To the best of our knowledge, the unrelated PTase by the type strains S. aculeolatus and S. synnematofor- CnqPT1 is the only non-ABBA PTase involved in the mans [9], which are the only named species within the production of a HI secondary metabolite. CnqPT1 is MAR4 lineage. membrane-bound and responsible for the O-prenylation MAR4 strains have previously been linked to the pro- of phenazine in the biosynthesis of marinophenazine in duction of secondary metabolites broadly classified as the MAR4 strain CNQ-509 [13]. hybrid isoprenoids (HIs) [10]. These compounds are bio- The isoprene used in bacterial terpenoid biosynthesis synthetic hybrids that derive part of their structures is derived from either the mevalonate (mev) or non- from five-carbon isoprene units. The addition of iso- mevalonate pathways [23]. Most bacteria, including prene (a process called “prenylation”) can occur on a Streptomyces, possess the non-mevalonate pathway, the variety of chemical scaffolds thus creating considerable products of which are used in the biosynthesis of structural diversity. HIs frequently possess biological primary metabolites such as respiratory ubiquinones activity and thus their discovery is of interest to the [24, 25]. In cases where bacteria also possess the mev pharmaceutical industry [11]. Based on literature re- pathway in addition to the non-mevalonate pathway, ports, HI production appears to be scattered throughout it has always been found flanking a HI gene cluster the Streptomyces phylogeny and is a relatively rare part [26] suggesting that the isoprene produced by this of secondary metabolism [10]. In contrast, some mem- biosynthetic route is used for secondary metabolism. bers of the MAR4 clade have been observed to produce Feeding experiments have confirmed that the mev up to three distinct classes of HI secondary metabolites pathwaycanprovidesomeoralloftheisoprenein- [10, 12, 13]. In addition, all MAR4 strains tested produce corporated into HI secondary metabolites [23, 27–30] at least one HI, an ability that has not been reported and led to the hypothesis that the mev pathway is a elsewhere in the Streptomyces genus [9]. To date, HI sec- marker for HI production [26]. The availability of a ondary metabolites produced by MAR4 strains include large number of Streptomyces genome sequences now naphthoquionones in the napyradiomycin [14] and mari- provides the opportunity to further explore the asso- none class [15, 16], the phthalazinone azamerone [17], ciation of the mev pathway with HI biosynthesis. the phenazines lavanducyanin [18] and marinophenazine To date, most evidence for the presence of HI path- [13], and the highly
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