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Abstract

Bacteria communicate by small-molecule chemicals that facilitate intra- and inter-species interactions. These extracellular signalling molecules mediate diverse processes including virulence, bioluminescence, biofilm formation, motility and specialized metabolism. The signalling molecules produced by members of the phylum Actinobacteria generally comprise γ-butyrolactones, γ-butenolides and furans. The best-known actinomycete γ-butyrolactone is A-factor, which triggers specialized metabolism and morphological differentiation in the genus . Salinipostins A–K are unique γ-butyrolactone molecules with rare phosphotriester moieties that were recently characterized from the marine actinomycete genus . The production of these compounds has been linked to the nine-gene biosynthetic gene cluster (BGC) . Critical to salinipostin assembly is the γ-butyrolactone synthase encoded by . Here, we report the surprising distribution of homologues across 12 bacterial phyla, the majority of which are not known to produce γ-butyrolactones. Further analyses uncovered a large group of -like gene clusters outside of the genus , suggesting the production of new salinipostin-like diversity. These gene clusters show evidence of horizontal transfer and location-specific recombination among strains. The results suggest that γ-butyrolactone production may be more widespread than previously recognized. The identification of new γ-butyrolactone BGCs is the first step towards understanding the regulatory roles of the encoded small molecules in Actinobacteria.

Funding
This study was supported by the:
  • Japan Society for Promotion of Science (Award JSPS Overseas Research Fellowship)
    • Principle Award Recipient: YutaKudo
  • National Institutes of Health (Award 5R01GM085770)
    • Principle Award Recipient: PaulR. Jensen
  • National Institutes of Health (Award 5R01GM085770)
    • Principle Award Recipient: BradleyS. Moore
  • National Science Foundation (Award DGE-1650112)
    • Principle Award Recipient: KaitlinE. Creamer
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2024-03-29
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References

  1. Papenfort K, Bassler BL. Quorum sensing signal–response systems in Gram-negative bacteria. Nat Rev Microbiol 2016; 14:576–588 [View Article][PubMed]
    [Google Scholar]
  2. Novick RP, Geisinger E. Quorum sensing in staphylococci. Annu Rev Genet 2008; 42:541–564 [View Article][PubMed]
    [Google Scholar]
  3. Khokhlov AS, Tovarova BLN, Pliner SA, Shevchenko LN, Kornitskaia EI et al. A-faktor, obespechivaiushchii biosintez streptomitsina mutantnym shtammom Actinomyces streptomycini. Dokl Akad Nauk SSSR 1967; 177:232–235
    [Google Scholar]
  4. Ando N, Matsumori N, Sakuda S, Beppu T, Horinouchi S. Involvement of AfsA in A-factor biosynthesis as a key enzyme. J Antibiot 1997; 50:847–852 [View Article][PubMed]
    [Google Scholar]
  5. Lee YJ, Kitani S, Nihira T. Null mutation analysis of an afsA-family gene, barX, that is involved in biosynthesis of the γ-butyrolactone autoregulator in Streptomyces virginiae. Microbiology 2010; 156:206–210 [View Article][PubMed]
    [Google Scholar]
  6. Sato K, Nihira T, Sakuda S, Yanagimoto M, Yamada Y. Isolation and structure of a new butyrolactone autoregulator from Streptomyces sp. FRI-5. J Ferment Bioeng 1989; 68:170–173 [View Article]
    [Google Scholar]
  7. Hashimoto K, Nihira T, Sakuda S, Yamada Y. IM-2, a butyrolactone autoregulator, induces production of several nucleoside antibiotics in Streptomyces sp. FRI-5. J Ferment Bioeng 1992; 73:449–455 [View Article]
    [Google Scholar]
  8. Kitani S, Yamada Y, Nihira T. Gene replacement analysis of the butyrolactone autoregulator receptor (FarA) reveals that FarA acts as a novel regulator in secondary metabolism of Streptomyces lavendulae FRI-5. J Bacteriol 2001; 183:4357–4363 [View Article][PubMed]
    [Google Scholar]
  9. Kitani S, Iida A, Izumi T, Maeda A, Yamada Y et al. Identification of genes involved in the butyrolactone autoregulator cascade that modulates secondary metabolism in Streptomyces lavendulae FRI-5. Gene 2008; 425:9–16 [View Article][PubMed]
    [Google Scholar]
  10. Waki M, Nihira T, Yamada Y. Cloning and characterization of the gene (farA) encoding the receptor for an extracellular regulatory factor (IM-2) from Streptomyces sp. strain FRI-5. J Bacteriol 1997; 179:5131–5137
    [Google Scholar]
  11. Gräfe U, Schade W, Eritt I, Fleck WF, Radics L. A new inducer of anthracycline biosynthesis from Streptomyces viridochromogenes. J Antibiot 1982; 35:1722–1723 [View Article][PubMed]
    [Google Scholar]
  12. Gräfe U, Reinhardt G, Schade W, Eritt I, Fleck WF et al. Interspecific inducers of cytodifferentiation and anthracycline biosynthesis from Streptomyces bikinensis and S. cyaneofuscatus. Biotechnol Lett 1983; 5:591–596
    [Google Scholar]
  13. Zou Z, Du D, Zhang Y, Zhang J, Niu G et al. A γ-butyrolactone-sensing activator/repressor, JadR3, controls a regulatory mini-network for jadomycin biosynthesis. Mol Microbiol 2014; 94:490–505
    [Google Scholar]
  14. Joo H-S, Yang Y-H, Lee C-S, Kim J-H, Kim B-G. Fragmentation study on butanolides with tandem mass spectrometry and its application for the screening of ScbR-captured quorum sensing molecules in Streptomyces coelicolor A3(2). Rapid Commun Mass Spectrom 2007; 21:764–770 [View Article][PubMed]
    [Google Scholar]
  15. Kato J, Funa N, Watanabe H, Ohnishi Y, Horinouchi S. Biosynthesis of y-butyrolactone autoregulators that switch on secondary metabolism and morphological development in Streptomyces. Proc Natl Acad Sci USA 2007; 104:2378–2383 [View Article][PubMed]
    [Google Scholar]
  16. Efremenkova OV. A-factor-like autoregulators. Russ J Bioorganic Chem 2016; 42:457–472
    [Google Scholar]
  17. Ceniceros A, Dijkhuizen L, Petrusma M. Molecular characterization of a Rhodococcus jostii RHA1 γ-butyrolactone(-like) signalling molecule and its main biosynthesis gene gblA. Sci Rep 2017; 7:17743 [View Article][PubMed]
    [Google Scholar]
  18. Onoprienko VV, Anisova LN, Blinova IN, Efremenkova OV, Koz’min YP. Bioregulators of Streptomyces coelicolor A3(2). In VII Sovetsko-Indiĭskiĭ Simpozium Po Khimii Prirodnykh Soedineniĭ Tbilisi: 1983 pp 111–112
    [Google Scholar]
  19. Takano E, Nihira T, Hara Y, Jones JJ, Gershater CJL et al. Purification and structural determination of SCB1, a gamma-butyrolactone that elicits antibiotic production in Streptomyces coelicolor A3(2). J Biol Chem 2000; 275:11010–11016
    [Google Scholar]
  20. Hsiao N-H, Söding J, Linke D, Lange C, Hertweck C et al. ScbA from Streptomyces coelicolor A3(2) has homology to fatty acid synthases and is able to synthesize γ-butyrolactones. Microbiology 2007; 153:1394–1404 [View Article][PubMed]
    [Google Scholar]
  21. Hsiao NH, Nakayama S, Merlo ME, de Vries M, Bunet R et al. Analysis of two additional signaling molecules in Streptomyces coelicolor and the development of a butyrolactone-specific reporter system. Chem Biol 2009; 16:951–960
    [Google Scholar]
  22. Sidda JD, Poon V, Song L, Wang W, Yang K et al. Overproduction and identification of butyrolactones SCB1-8 in the antibiotic production superhost: Streptomyces M1152. Org Biomol Chem 2016; 14:6390–6393
    [Google Scholar]
  23. Yamada Y, Sugamura K, Kondo K, Yanagimoto M, Okada H. The structure of inducing factors for virginiamycin production in Streptomyces virginiae. J Antibiot 1987; 40:496–504 [View Article][PubMed]
    [Google Scholar]
  24. Kondo K, Higuchi Y, Sakuda S, Nihira T, Yamada Y. New virginiae butanolides from Streptomyces virginiae. J Antibiot 1989; 42:1873–1876 [View Article][PubMed]
    [Google Scholar]
  25. Kawachi R, Akashi T, Kamitani Y, Sy A, Wangchaisoonthorn U et al. Identification of an AfsA homologue (BarX) from Streptomyces virginiae as a pleiotropic regulator controlling autoregulator biosynthesis, virginiamycin biosynthesis and virginiamycin M1 resistance. Mol Microbiol 2000; 36:302–313
    [Google Scholar]
  26. Arakawa K, Mochizuki S, Yamada K, Noma T, Kinashi H. γ-Butyrolactone autoregulator-receptor system involved in lankacidin and lankamycin production and morphological differentiation in Streptomyces rochei. Microbiology 2007; 153:1817–1827
    [Google Scholar]
  27. Arakawa K, Tsuda N, Taniguchi A, Kinashi H. The butenolide signaling molecules SRB1 and SRB2 induce lankacidin and lankamycin production in Streptomyces rochei. Chembiochem 2012; 13:1447–1457 [View Article][PubMed]
    [Google Scholar]
  28. Yamamoto S, He Y, Arakawa K, Kinashi H. γ-Butyrolactone-dependent expression of the Streptomyces antibiotic regulatory protein gene srrY plays a central role in the regulatory cascade leading to lankacidin and lankamycin production in Streptomyces rochei. J Bacteriol 2008; 190:1308–1316 [View Article][PubMed]
    [Google Scholar]
  29. Kitani S, Miyamoto KT, Takamatsu S, Herawati E, Iguchi H et al. Avenolide, a Streptomyces hormone controlling antibiotic production in Streptomyces avermitilis. Proc Natl Acad Sci USA 2011; 108:16410–16415 [View Article][PubMed]
    [Google Scholar]
  30. Zhu J, Sun D, Liu W, Chen Z, Li J et al. AvaR2, a pseudo γ-butyrolactone receptor homologue from Streptomyces avermitilis, is a pleiotropic repressor of avermectin and avenolide biosynthesis and cell growth. Mol Microbiol 2016; 102:562–578
    [Google Scholar]
  31. Corre C, Song L, O'Rourke S, Chater KF, Challis GL. 2-Alkyl-4-hydroxymethylfuran-3-carboxylic acids, antibiotic production inducers discovered by Streptomyces coelicolor genome mining. Proc Natl Acad Sci USA 2008; 105:17510–17515 [View Article][PubMed]
    [Google Scholar]
  32. Sidda JD, Corre C. Gamma-butyrolactone and furan signaling systems in Streptomyces. Methods Enzymol 2012; 517:71–87 [View Article][PubMed]
    [Google Scholar]
  33. Recio E, Colinas A, Rumbero A, Aparicio JF, Martín JF. PI factor, a novel type quorum-sensing inducer elicits pimaricin production in Streptomyces natalensis. J Biol Chem 2004; 279:41586–41593 [View Article][PubMed]
    [Google Scholar]
  34. Matselyukh B, Mohammadipanah F, Laatsch H, Rohr J, Efremenkova O et al. N-methylphenylalanyl-dehydrobutyrine diketopiperazine, an A-factor mimic that restores antibiotic biosynthesis and morphogenesis in Streptomyces globisporus 1912-B2 and Streptomyces griseus 1439. J Antibiot 2015; 68:9–14 [View Article][PubMed]
    [Google Scholar]
  35. Horinouchi S. A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front Biosci 2002; 7:d2045-57[PubMed]
    [Google Scholar]
  36. Takano E. γ-Butyrolactones: Streptomyces signalling molecules regulating antibiotic production and differentiation. Curr Opin Microbiol 2006; 9:287–294
    [Google Scholar]
  37. Nishida H, Ohnishi Y, Beppu T, Horinouchi S. Evolution of γ-butyrolactone synthases and receptors in Streptomyces. Environ Microbiol 2007; 9:1986–1994 [View Article][PubMed]
    [Google Scholar]
  38. Willey JM, Gaskell AA. Morphogenetic signaling molecules of the streptomycetes. Chem Rev 2011; 111:174–187 [View Article][PubMed]
    [Google Scholar]
  39. Polkade AV, Mantri SS, Patwekar UJ, Jangid K. Quorum sensing: An under-explored phenomenon in the phylum Actinobacteria. Front Microbiol 2016; 7:131 [View Article][PubMed]
    [Google Scholar]
  40. Niu G, Chater KF, Tian Y, Zhang J, Tan H. Specialised metabolites regulating antibiotic biosynthesis in Streptomyces spp. FEMS Microbiol Rev 2016; 40:554–573 [View Article][PubMed]
    [Google Scholar]
  41. Daniel-Ivad M, Pimentel-Elardo S, Nodwell JR. Control of specialized metabolism by signaling and transcriptional regulation: opportunities for new platforms for drug discovery?. Annu Rev Microbiol 2018; 72:25–48
    [Google Scholar]
  42. Lee KM, Lee C-K, Choi S-U, Park H-R, Kitani S et al. Cloning and in vivo functional analysis by disruption of a gene encoding the γ-butyrolactone autoregulator receptor from Streptomyces natalensis. Arch Microbiol 2005; 184:249–257
    [Google Scholar]
  43. Healy FG, Eaton KP, Limsirichai P, Aldrich JF, Plowman AK et al. Characterization of γ-butyrolactone autoregulatory signaling gene homologs in the angucyclinone polyketide WS5995B producer Streptomyces acidiscabies. J Bacteriol 2009; 191:4786–4797
    [Google Scholar]
  44. Choi S-U, Lee C-K, Hwang Y-I, Kinoshita H, Nihira T. Cloning and functional analysis by gene disruption of a gene encoding a γ-butyrolactone autoregulator receptor from Kitasatospora setae. J Bacteriol 2004; 186:3423–3430 [View Article][PubMed]
    [Google Scholar]
  45. Ichikawa N, Oguchi A, Ikeda H, Ishikawa J, Kitani S et al. Genome sequence of Kitasatospora setae NBRC 14216T: an evolutionary snapshot of the family Streptomycetaceae. DNA Res 2010; 17:393–406 [View Article][PubMed]
    [Google Scholar]
  46. Aroonsri A, Kitani S, Hashimoto J, Kosone I, Izumikawa M et al. Pleiotropic control of secondary metabolism and morphological development by KsbC, a butyrolactone autoregulator receptor homologue in Kitasatospora setae. Appl Environ Microbiol 2012; 78:8015–8024 [View Article][PubMed]
    [Google Scholar]
  47. Intra B, Euanorasetr J, Nihira T, Panbangred W. Characterization of a gamma-butyrolactone synthetase gene homologue (stcA) involved in bafilomycin production and aerial mycelium formation in Streptomyces sp. SBI034. Appl Microbiol Biotechnol 2016; 100:2749–2760
    [Google Scholar]
  48. Salehi-Najafabadi Z, Barreiro C, Rodríguez-García A, Cruz A, López GE et al. The gamma-butyrolactone receptors BulR1 and BulR2 of Streptomyces tsukubaensis: tacrolimus (FK506) and butyrolactone synthetases production control. Appl Microbiol Biotechnol 2014; 98:4919–4936
    [Google Scholar]
  49. Tan G-Y, Peng Y, Lu C, Bai L, Zhong J-J. Engineering validamycin production by tandem deletion of γ-butyrolactone receptor genes in Streptomyces hygroscopicus 5008. Metab Eng 2015; 28:74–81 [View Article][PubMed]
    [Google Scholar]
  50. Choi S-U, Lee C-K, Hwang Y-I, Kinosita H, Nihira T. γ-Butyrolactone autoregulators and receptor proteins in non-Streptomyces actinomycetes producing commercially important secondary metabolites. Arch Microbiol 2003; 180:303–307
    [Google Scholar]
  51. Du Y-L, Shen X-L, Yu P, Bai L-Q, Li Y-Q. Gamma-butyrolactone regulatory system of Streptomyces chattanoogensis links nutrient utilization, metabolism, and development. Appl Environ Microbiol 2011; 77:8415–8426 [View Article][PubMed]
    [Google Scholar]
  52. Millán-Aguiñaga N, Chavarria KL, Ugalde JA, Letzel A-C, Rouse GW et al. Phylogenomic insight into Salinispora (bacteria, actinobacteria) species designations. Sci Rep 2017; 7:3564 [View Article][PubMed]
    [Google Scholar]
  53. Román-Ponce B, Millán-Aguiñaga N, Guillen-Matus D, Chase AB, Ginigini JGM et al. Six novel species of the obligate marine actinobacterium Salinispora, Salinispora cortesiana sp. nov., Salinispora fenicalii sp. nov., Salinispora goodfellowii sp. nov., Salinispora mooreana sp. nov., Salinispora oceanensis sp. nov. and Salinispora vitiensis sp. nov., and emended description of the genus Salinispora. Int J Syst Evol Microbiol 2020; 70:4668–4682 [View Article][PubMed]
    [Google Scholar]
  54. Mincer TJ, Jensen PR, Kauffman CA, Fenical W. Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 2002; 68:5005–5011
    [Google Scholar]
  55. Jensen PR, Gontang E, Mafnas C, Mincer TJ, Fenical W. Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environ Microbiol 2005; 7:1039–1048 [View Article][PubMed]
    [Google Scholar]
  56. Mincer TJ, Fenical W, Jensen PR. Culture-dependent and culture-independent diversity within the obligate marine actinomycete genus Salinispora. Appl Environ Microbiol 2005; 71:7019–7028
    [Google Scholar]
  57. Maldonado LA, Fenical W, Jensen PR, Kauffman CA, Mincer TJ et al. Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae. Int J Syst Evol Microbiol 2005; 55:1759–1766
    [Google Scholar]
  58. Kim TK, Garson MJ, Fuerst JA. Marine actinomycetes related to the ‘Salinospora’ group from the Great Barrier Reef sponge Pseudoceratina clavata. Environ Microbiol 2005; 7:509–518
    [Google Scholar]
  59. Vidgen ME, Hooper JNA, Fuerst JA. Diversity and distribution of the bioactive actinobacterial genus Salinispora from sponges along the Great Barrier Reef. Antonie Van Leeuwenhoek 2012; 101:603–618 [View Article][PubMed]
    [Google Scholar]
  60. Jensen PR, Moore BS, Fenical W. The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery. Nat Prod Rep 2015; 32:738–751
    [Google Scholar]
  61. Feling RH, Buchanan GO, Mincer TJ, Kauffman CA, Jensen PR et al. Salinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus salinospora. Angew Chem Int Ed Engl 2003; 42:355–357 [View Article][PubMed]
    [Google Scholar]
  62. Letzel A-C, Li J, Amos GCA, Millán-Aguiñaga N, Ginigini J et al. Genomic insights into specialized metabolism in the marine actinomycete Salinispora. Environ Microbiol 2017; 19:3660–3673
    [Google Scholar]
  63. Amos GCA, Awakawa T, Tuttle RN, Letzel A-C, Kim MC et al. Comparative transcriptomics as a guide to natural product discovery and biosynthetic gene cluster functionality. Proc Natl Acad Sci USA 2017; 114:E11121–E11130 [View Article][PubMed]
    [Google Scholar]
  64. Schulze CJ, Navarro G, Ebert D, DeRisi J, Linington RG. Salinipostins A-K, long-chain bicyclic phosphotriesters as a potent and selective antimalarial chemotype. J Org Chem 2015; 80:1312–1320 [View Article][PubMed]
    [Google Scholar]
  65. Yoo E, Schulze CJ, Stokes BH, Onguka O, Yeo T et al. The antimalarial natural product salinipostin A identifies essential α/β serine hydrolases involved in lipid metabolism in P. falciparum parasites. Cell Chem Biol 2020; 27:143–157 [View Article][PubMed]
    [Google Scholar]
  66. Schlawis C, Kern S, Kudo Y, Grunenberg J, Moore BS et al. Structural elucidation of trace components combining GC/MS, GC/IR, DFT-calculation and synthesis – salinilactones, unprecedented bicyclic lactones from Salinispora bacteria. Angew Chem Int Ed Engl 2018; 57:14921–14925 [View Article][PubMed]
    [Google Scholar]
  67. Schlawis C, Harig T, Ehlers S, Guillen-Matus DG, Creamer KE et al. Extending the salinilactone family. Chembiochem 2020; 21:1629–1632 [View Article][PubMed]
    [Google Scholar]
  68. Kudo Y, Awakawa T, Du Y-L, Jordan PA, Creamer KE et al. Expansion of gamma-butyrolactone signaling molecule biosynthesis to phosphotriester natural products. ACS Chem Biol 2020; 15:3253–3261 [View Article][PubMed]
    [Google Scholar]
  69. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 2017; 45:D200–D203
    [Google Scholar]
  70. Mendler K, Chen H, Parks DH, Lobb B, Hug LA et al. AnnoTree: visualization and exploration of a functionally annotated microbial tree of life. Nucleic Acids Res 2019; 47:4442–4448
    [Google Scholar]
  71. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402
    [Google Scholar]
  72. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649
    [Google Scholar]
  73. Hadjithomas M, Chen I-MA, Chu K, Huang J, Ratner A et al. IMG-ABC: new features for bacterial secondary metabolism analysis and targeted biosynthetic gene cluster discovery in thousands of microbial genomes. Nucleic Acids Res 2017; 45:D560–D565
    [Google Scholar]
  74. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ et al. antiSMASH 4.0 – improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 2017; 45:W36–W41 [View Article]
    [Google Scholar]
  75. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87
    [Google Scholar]
  76. Medema MH, Takano E, Breitling R. Detecting sequence homology at the gene cluster level with MultiGeneBlast. Mol Biol Evol 2013; 30:1218–1223
    [Google Scholar]
  77. Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 2019; 47:D607–D613
    [Google Scholar]
  78. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797
    [Google Scholar]
  79. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis, 3.40 2018 http://www.mesquiteproject.org
  80. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165
    [Google Scholar]
  81. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313
    [Google Scholar]
  82. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321
    [Google Scholar]
  83. Lefort V, Longueville JE, Gascuel O. SMS: smart model selection in PhyML. Mol Biol Evol 2017; 34:2422–2424
    [Google Scholar]
  84. Ziemert N, Lechner A, Wietz M, Millán-Aguiñaga N, Chavarria KL et al. Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora. Proc Natl Acad Sci USA 2014; 111:E1130–1139
    [Google Scholar]
  85. Rambaut A. FigTree v1.4.3 2016 https://github.com/rambaut/figtree/releases
  86. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259
    [Google Scholar]
  87. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:2007 [View Article][PubMed]
    [Google Scholar]
  88. Dillon SC, Bateman A. The hotdog fold: wrapping up a superfamily of thioesterases and dehydratases. BMC Bioinformatics 2004; 5:109
    [Google Scholar]
  89. Chen I-MA, Chu K, Palaniappan K, Pillay M, Ratner A et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res 2018; 47:666–677
    [Google Scholar]
  90. Enright AJ, Iliopoulos I, Kyrpides NC, Ouzounis CA. Protein interaction maps for complete genomes based on gene fusion events. Nature 1999; 402:86–90
    [Google Scholar]
  91. Marcotte EM, Pellegrini M, Ng HL, Rice DW, Yeates TO et al. Detecting protein function and protein–protein interactions from genome sequences. Science 1999; 285:751–753 [View Article][PubMed]
    [Google Scholar]
  92. Penn K, Jenkins C, Nett M, Udwary DW, Gontang EA et al. Genomic islands link secondary metabolism to functional adaptation in marine actinobacteria. ISME J 2009; 3:1193–1203 [View Article][PubMed]
    [Google Scholar]
  93. Ziemert N, Podell S, Penn K, Badger JH, Allen E et al. The natural product domain seeker NaPDoS: a phylogeny based bioinformatic tool to classify secondary metabolite gene diversity. PLoS One 2012; 7:e34064
    [Google Scholar]
  94. Van Santen JA, Jacob G, Singh AL, Aniebok V, Balunas MJ et al. The Natural Products Atlas: an open access knowledge base for microbial natural products discovery. ACS Cent Sci 2019; 5:1824–1833 [View Article][PubMed]
    [Google Scholar]
  95. Kautsar SA, Blin K, Shaw S, Navarro-Muñoz JC, Terlouw BR et al. MIBiG 2.0: a repository for biosynthetic gene clusters of known function. Nucleic Acids Res 2020; 48:D454–D458
    [Google Scholar]
  96. Chevrette MG, Gutiérrez-García K, Selem-Mojica N, Aguilar-Martínez C, Yañez-Olvera A et al. Evolutionary dynamics of natural product biosynthesis in bacteria. Nat Prod Rep 2020; 37:566–599
    [Google Scholar]
  97. Niehs SP, Kumpfmüller J, Dose B, Little RF, Ishida K et al. Insect‐associated bacteria assemble the antifungal butenolide gladiofungin by non-canonical polyketide chain termination. Angew Chem Int Ed Engl 2020; 59:23122–23126 [View Article][PubMed]
    [Google Scholar]
  98. Nakou IT, Jenner M, Dashti Y, Romero-Canelón I, Masschelein J et al. Genomics-driven discovery of a novel glutarimide antibiotic from Burkholderia gladioli reveals an unusual polyketide synthase chain release mechanism. Angew Chem Int Ed Engl 2020; 59:23145–23153 [View Article][PubMed]
    [Google Scholar]
  99. de Rond T, Asay JE, Moore BS. Co-occurrence of enzyme domains guides the discovery of an oxazolone synthetase. bioRxiv 2020147165 [View Article]
    [Google Scholar]
  100. Park CJ, Smith JT, Andam CP. Horizontal gene transfer and genome evolution in the phylum Actinobacteria. Horizontal Gene Transfer Cham: Springer; 2019 pp 155–174
    [Google Scholar]
  101. Bruns H, Crüsemann M, Letzel A-C, Alanjary M, McInerney JO et al. Function-related replacement of bacterial siderophore pathways. ISME J 2018; 12:320–329 [View Article][PubMed]
    [Google Scholar]
  102. Bose U, Ortori CA, Sarmad S, Barrett DA, Hewavitharana AK et al. Production of N-acyl homoserine lactones by the sponge-associated marine actinobacteria Salinispora arenicola and Salinispora pacifica. FEMS Microbiol Lett 2017; 364:fnx002 [View Article]
    [Google Scholar]
  103. McBride SG, Strickland MS. Quorum sensing modulates microbial efficiency by regulating bacterial investment in nutrient acquisition enzymes. Soil Biol Biochem 2019; 136:107514 [View Article]
    [Google Scholar]
  104. Patteson JB, Lescallette AR, Li B. Discovery and biosynthesis of azabicyclene, a conserved nonribosomal peptide in Pseudomonas aeruginosa. Org Lett 2019; 21:4955–4959 [View Article][PubMed]
    [Google Scholar]
  105. Okada BK, Seyedsayamdost MR. Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules. FEMS Microbiol Rev 2017; 41:19–33 [View Article][PubMed]
    [Google Scholar]
  106. Alberti F, Leng DJ, Wilkening I, Song L, Tosin M et al. Triggering the expression of a silent gene cluster from genetically intractable bacteria results in scleric acid discovery. Chem Sci 2019; 10:453–463 [View Article][PubMed]
    [Google Scholar]
  107. Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE et al. The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 2019; 10:516 [View Article][PubMed]
    [Google Scholar]
  108. Okamura H, Fujioka T, Mori N, Taniguchi T, Monde K et al. First enantioselective synthesis of salinipostin A, a marine cyclic enol-phosphotriester isolated from Salinispora sp. Tetrahedron Lett 2019; 60:150917 [View Article]
    [Google Scholar]
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