Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters

Microbiology (United Kingdom)

Volumn 162, Issue 12, 2016, Pages 2075-2086

  Schorn, Michelle A ^a   Alanjary, Mohammad M ^b   Aguinaldo, Kristen ^c   Korobeynikov, Anton ^d   Podell, Sheila ^a   Patin, Nastassia ^a   Lincecum, Tommie ^c   Jensen, Paul R ^a,e   Ziemert, Nadine ^b   Moore, Bradley S ^a,e,f  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c Thermo Fisher Scientific   (United States)

^d ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Gene cluster similarity network; Genome mining; Genome sequencing; Marine actinomycetes; Secondary metabolites

Indexed keywords

NATURAL PRODUCT; RNA 16S; BACTERIAL PROTEIN; BIOLOGICAL PRODUCT; SEA WATER;

ACTINOBACTERIA; ACTINOMADURA; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM; BIOSYNTHESIS; CORYNEBACTERIUM; DNA BASE COMPOSITION; EDITORIAL; GENE CLUSTER; GENOME ANALYSIS; GENOME SIZE; GORDONIA; HETEROLOGOUS EXPRESSION; METABOLITE; MICROCOCCINEAE; MICROMONOSPORA; NEXT GENERATION SEQUENCING; NOCARDIA; NOCARDIOPSIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PSEUDONOCARDIA; RHODOCOCCUS; SACCHAROMONOSPORA; SALINISPORA; SEQUENCE ANALYSIS; SEQUENCE DATABASE; SEQUENCE HOMOLOGY; STREPTOMYCES; DENSITY; GENE SEQUENCE; GENETIC VARIABILITY; MARINE SPECIES; CLASSIFICATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY;

ACTINOBACTERIA; BACTERIAL PROTEINS; BIOLOGICAL PRODUCTS; GENOME, BACTERIAL; PHYLOGENY; SEAWATER; SEQUENCE ANALYSIS, DNA;

EID: 85007400490     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000386     Document Type: Editorial

References (64)

1. Abdel-Mageed, W. M., Milne, B. F., Wagner, M., Schumacher, M., Sandor, P., Pathom-aree, W., Goodfellow, M., Bull, A. T., Horikoshi, K. & other authors (2010). Dermacozines, a new phenazine family from deep-sea dermacocci isolated from a Mariana Trench sediment. Org Biomol Chem 8, 2352-2362.
2. Bachmann, B. O., Van Lanen, S. G. & Baltz, R. H. (2014). Microbial genome mining for accelerated natural products discovery: is a renaissance in the making? J Ind Microbiol Biotechnol 41, 175-184.
3. Baltz, R. H. (2006). Marcel Faber Roundtable: is our antibiotic pipeline unproductive because of starvation, constipation or lack of inspiration? J Ind Microbiol Biotechnol 33, 507-513.
4. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S. & other authors (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19, 455-477.
5. Bastian, M., Heymann, S. & Jacomy, M. (2009). Gephi: an open source software for exploring and manipulating networks. In Third International AAAI Conference on Weblogs and Social Media. San Jose McEnery Convention Center.
6. Bennur, T., Ravi Kumar, A., Zinjarde, S. S. & Javdekar, V. (2016). Nocardiopsis species: a potential source of bioactive compounds. J Appl Microbiol 120, 1-16.
7. Bentley, S. D., Chater, K. F., Cerdeño-Tarraga, A. M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H. & other authors (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141-147.
8. Berdy, J. (2005). Bioactive microbial metabolites. J Antibiot 58, 1-26
9. Berdy, J. (2012). Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65, 441.
10. Brader, G., Compant, S., Mitter, B., Trognitz, F. & Sessitsch, A. (2014). Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27, 30-37
11. Cane, D. E. & Ikeda, H. (2012). Exploration and mining of the bacterial terpenome. Acc Chem Res 45, 463-472.
12. Capella-Gutierrez, S., Silla-Martínez, J. M. & Gabaldón, T. (2009). tri-mAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973.
13. Choi, S.-S., Kim, H.-J., Lee, H.-S., Kim, P. & Kim, E.-S. (2015). Genome mining of rare actinomycetes and cryptic pathway awakening. Process Biochem 50, 1184-1193.
14. Chavez, R., Fierro, F., García-Rico, R. O. & Vaca, I. (2015). Filamentous fungi from extreme environments as a promising source of novel bioactive secondary metabolites. Front Microbiol 6, 903.
15. Cimermancic, P., Medema, M. H., Claesen, J., Kurita, K., Wieland Brown, L. C., Mavrommatis, K., Pati, A., Godfrey, P. A., Koehrsen, M. & other authors (2014). Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters. Cell 158, 412-421.
16. Doroghazi, J. R. & Metcalf, W. W. (2013). Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes. BMC Genomics 14, 611.
17. Doroghazi, J. R., Albright, J. C., Goering, A. W., Ju, K. S., Haines, R. R., Tchalukov, K. A., Labeda, D. P., Kelleher, N. L. & Metcalf, W. W. (2014). A roadmap for natural product discovery based on large-scale genomics and metabolomics. Nat Chem Biol 10, 963-968.
18. Eltamany, E. E., Abdelmohsen, U. R., Ibrahim, A. K., Hassanean, H. A., Hentschel, U. & Ahmed, S. A. (2014). New antibacterial xanthone from the marine sponge-derived Micrococcus sp. EG45. Bioorg Med Chem Lett 24, 4939-4942.
19. Eustaquio, A. S., Nam, S.-J., Penn, K., Lechner, A., Wilson, M. C., Fenical, W., Jensen, P. R. & Moore, B. S. (2011). The discovery of Salinosporamide K from the marine bacterium Salinispora pacifica by genome mining gives insight into pathway evolution. ChemBioChem 12, 61-64
20. Fenical, W. & Jensen, P. R. (2006). Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2, 666-673.
21. Gomez-Escribano, J., Alt, S. & Bibb, M. (2016). Next generation sequencing of Actinobacteria for the discovery of novel natural products. Mar Drugs 14, 78.
22. Gontang, E. A., Fenical, W. & Jensen, P. R. (2007). Phylogenetic diversity of Gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73, 3272-3282.
23. Gontang, E. A., Gaudencio, S. P., Fenical, W. & Jensen, P. R. (2010). Sequence-based analysis of secondary-metabolite biosynthesis in marine Actinobacteria. Appl Environ Microbiol 76, 2487-2499.
24. Hadjithomas, M., Chen, I. M., Chu, K., Ratner, A., Palaniappan, K., Szeto, E., Huang, J., Reddy, T. B., Cimermancic, P. & other authors (2015). IMG-ABC: a knowledge base to fuel discovery of biosynthetic gene clusters and novel secondary metabolites. MBio 6, e00932-15.
25. Hu, Y. (2006). Efficient, high-quality force-directed graph drawing. Mathematica J 10, 37-71.
26. Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Hattori, M. & Omura, S. (2003). Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21, 526-531.
27. Jensen, P. R., Gontang, E., Mafnas, C., Mincer, T. J. & Fenical, W. (2005). Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environ Microbiol 7, 1039-1048.
28. Jensen, P. R., Chavarria, K. L., Fenical, W., Moore, B. S. & Ziemert, N. (2014). Challenges and triumphs to genomics-based natural product discovery. J Ind Microbiol Biotechnol 41, 203-209.
29. Jensen, P. R., Moore, B. S. & Fenical, W. (2015). The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery. Nat Prod Rep 32, 738-751.
30. Jost, L. (2006). Entropy and diversity. Oikos 113, 363-375
31. Katoh, K., Kuma, K.-I., Toh, H. & Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33, 511-518.
32. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J. & Marra, M. A. (2009). Circos: an information aesthetic for comparative genomics. Genome Res 19, 1639-1645.
33. Land, M. L., Hyatt, D., Jun, S. R., Kora, G. H., Hauser, L. J., Lukjancenko, O. & Ussery, D. W. (2014). Quality scores for 32,000 genomes. Stand Genomic Sci 9, 20.
34. Lazzarini, A., Cavaletti, L., Toppo, G. & Marinelli, F. (2001). Rare genera of actinomycetes as potential producers of new antibiotics. Antonie Van Leeuwenhoek 79, 399-405.
35. Letunic, I. & Bork, P. (2016). Interactive Tree of Life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44, W242-W245.
36. Lin, K., Zhu, L. & Zhang, D. Y. (2006). An initial strategy for comparing proteins at the domain architecture level. Bioinformatics 22, 2081-2086.
37. Manivasagan, P., Venkatesan, J., Sivakumar, K. & Kim, S. K. (2014). Pharmaceutically active secondary metabolites of marine actinobacteria. Microbiol Res 169, 262-278.
38. Medema, M. H. & Fischbach, M. A. (2015). Computational approaches to natural product discovery. Nat Chem Biol 11, 639-648.
39. Medema, M. H., Takano, E. & Breitling, R. (2013). Detecting sequence homology at the gene cluster level with MultiGeneBlast. Mol Biol Evol 30, 1218-1223.
40. Medema, M. H., Kottmann, R., Yilmaz, P., Cummings, M., Biggins, J. B., Blin, K., de Bruijn, I., Chooi, Y. H., Claesen, J. & other authors (2015). Minimum information about a biosynthetic gene cluster. Nat Chem Biol 11, 625-631.
41. Monciardini, P., Iorio, M., Maffioli, S., Sosio, M. & Donadio, S. (2014). Discovering new bioactive molecules from microbial sources. Microb Biotechnol 7, 209-220.
42. Moore, B. S., Kalaitzis, J. A. & Xiang, L. (2005). Exploiting marine actinomycete biosynthetic pathways for drug discovery. Antonie van Leeuwenhoek 87, 49-57.
43. Nett, M., Ikeda, H. & Moore, B. S. (2009). Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26, 1362-1384.
44. Nurk, S., Bankevich, A., Antipov, D., Gurevich, A. A., Korobeynikov, A., Lapidus, A., Prjibelski, A. D., Pyshkin, A., Sirotkin, A. & other authors (2013). Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20, 714-737.
45. Nylander, J. A. A. (2004). MrModeltest v2. Evolutionary Biology Centre, Uppsala University: Program distributed by the author.
46. Palomo, S., Gonzalez, I., de la Cruz, M., Martín, J., Tormo, J. R., Anderson, M., Hill, R. T., Vicente, F., Reyes, F. & other authors (2013). Sponge-derived Kocuria and Micrococcus spp. as sources of the new thiazolyl peptide antibiotic Kocurin. Mar Drugs 11, 1071-1086.
47. Podell, S. & Gaasterland, T. (2007). DarkHorse: a method for genomewide prediction of horizontal gene transfer. Genome Biol 8, R16.
48. Rothberg, J. M., Hinz, W., Rearick, T. M., Schultz, J., Mileski, W., Davey, M., Leamon, J. H., Johnson, K., Milgrew, M. J. & other authors (2011). An integrated semiconductor device enabling non-optical genome sequencing. Nature 475, 348-352.
49. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
50. Subramani, R. & Aalbersberg, W. (2013). Culturable rare Actinomycetes: diversity, isolation and marine natural product discovery. Appl Microbiol Biotechnol 97, 9291-9321.
51. Tang, X., Li, J., Millan-Aguiñaga, N., Zhang, J. J., O’Neill, E. C., Ugalde, J. A., Jensen, P. R., Mantovani, S. M. & Moore, B. S. (2015). Identification of thiotetronic acid antibiotic biosynthetic pathways by target-directed genome mining. ACS Chem Biol 10, 2841-2849.
52. Tiwari, K. & Gupta, R. K. (2012). Rare actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 32, 108-132.
53. Trzoss, L., Fukuda, T., Costa-Lotufo, L. V., Jimenez, P., La Clair, J. J. & Fenical, W. (2014). Seriniquinone, a selective anticancer agent, induces cell death by autophagocytosis, targeting the cancer-protective protein dermcidin. Proc Natl Acad Sci U S A 111, 14687-14692.
54. Tuomisto, H. (2010). A consistent terminology for quantifying species diversity? Yes, it does exist. Oecologia 164, 853-860.
55. Udwary, D. W., Zeigler, L., Asolkar, R. N., Singan, V., Lapidus, A., Fenical, W., Jensen, P. R. & Moore, B. S. (2007). Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc Natl Acad Sci U S A 104, 10376-10381.
56. Wagner, M., Abdel-Mageed, W. M., Ebel, R., Bull, A. T., Goodfellow, M., Fiedler, H. P. & Jaspars, M. (2014). Dermacozines H-J isolated from a deep-sea strain of Dermacoccus abyssi from Mariana Trench sediments. J Nat Prod 77, 416-420.
57. Weber, T., Blin, K., Duddela, S., Krug, D., Kim, H. U., Bruccoleri, R., Lee, S. Y., Fischbach, M. A., Müller, R. & other authors (2015). antiSMASH 3.0 a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43, W237-W243.
58. Yamada, Y., Kuzuyama, T., Komatsu, M., Shin-ya, K., Omura, S., Cane, D. E. & Ikeda, H. (2015). Terpene synthases are widely distributed in bacteria. Proc Natl Acad Sci U S A 112, 857-862.
59. Yamanaka, K., Reynolds, K. A., Kersten, R. D., Ryan, K. S., Gonzalez, D. J., Nizet, V., Dorrestein, P. C. & Moore, B. S. (2014). Direct cloning and refactoring of a silent lipopeptide biosynthetic gene cluster yields the antibiotic taromycin A. Proc Natl Acad Sci U S A 111, 1957-1962.
60. Yang, X.-W., Zhang, G.-Y., Ying, J.-X., Yang, B., Zhou, X.-F., Steinmetz, A., Liu, Y.-H. & Wang, N. (2013). Isolation, characterization, and bioactivity evaluation of 3-((6-methylpyrazin-2-yl)methyl)-1H-indole, a new alkaloid from a deep-sea-derived actinomycete Serinicoccus profundi sp. nov. Mar Drugs 11, 33-39.
61. Zhao, X. & Yang, T. (2011). Draft genome sequence of the marine sediment-derived actinomycete Streptomyces xinghaiensis NRRL B24674T. J Bacteriol 193, 5543.
62. Ziemert, N., Podell, S., Penn, K., Badger, J. H., Allen, E. & Jensen, P. R. (2012). The natural product domain seeker NaPDoS: a phylogeny based bioinformatic tool to classify secondary metabolite gene diversity. PLoS One 7, e34064.
63. Ziemert, N., Lechner, A., Wietz, M., Millan-Aguinaga, N., Chavarria, K. L. & Jensen, P. R. (2014). Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora. Proc Natl Acad Sci U S A 111, E1130-E1139.
64. Zotchev, S. B. (2012). Marine actinomycetes as an emerging resource for the drug development pipelines. J Biotechnol 158, 168-175.