Genome mining for natural product biosynthetic gene clusters in the Subsection V cyanobacteria

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Micallef, Melinda L ^a   D'Agostino, Paul M ^a,b   Sharma, Deepti ^c   Viswanathan, Rajesh ^c   Moffitt, Michelle C ^a  

^a UNIVERSITY OF WESTERN SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; CYANOBACTIN; HAPALINDOLE; HAPALOSIN; HYDROCARBON; MICROCYSTIN; MICROVIRIDIN; MYCOSPORINE LIKE AMINO ACID; NATURAL PRODUCT; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYKETIDE SYNTHASE; SCYTONEMIN; TERPENE; UNCLASSIFIED DRUG; WELWITINDOLINONE; BACTERIAL PROTEIN; BIOLOGICAL PRODUCT; PEPTIDE SYNTHASE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; CYANOBACTERIUM; DATA MINING; GENE CLUSTER; HAPALOSIPHON WELWITSCHII; NONHUMAN; PEPTIDE SYNTHESIS; POSTRIBOSOMAL PEPTIDE SYNTHESIS; WESTIELLA INTRICATA; AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; SECONDARY METABOLISM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOLOGICAL PRODUCTS; BIOSYNTHETIC PATHWAYS; CYANOBACTERIA; GENOME, BACTERIAL; HYDROCARBONS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDE SYNTHASES; SECONDARY METABOLISM; TERPENES;

EID: 84940531115     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1855-z     Document Type: Article

References (96)

1. Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, et al. Genomes of Stigonematalean cyanobacteria (Subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol. 2013;5(1):31-44.
2. Namikoshi M, Rinehart KL. Bioactive compounds produced by cyanobacteria. J Ind Microbiol Biotechnol. 1996;17(5-6):373-84.
3. Burja AM, Banaigs B, Abou-Mansour E, Grant Burgess J, Wright PC. Marine cyanobacteria-a prolific source of natural products. Tetrahedron. 2001;57(46):9347-77.
4. Welker M, Döhren H. Cyanobacterial peptides - nature's own combinatorial biosynthesis. FEMS Microbiol Rev. 2006;30(4):530-63.
5. Bhat V, Dave A, MacKay JA, Rawal VH: Chapter Two - The chemistry of hapalindoles, fischerindoles, ambiguines, and welwitindolinones. In: The Alkaloids: Chemistry and Biology. Edited by Hans-Joachim K, vol. Volume 73: New York, Academic Press; 2014: 65-160.
6. Moffitt MC, Burns BP: Hapalindole family of cyanobacterial natural products: structure, biosynthesis and function. In: Handbook on Cyanobacteria Edited by Gault PM, Marler HJ: New York, Nova Science Publishers, Inc; 2009
7. Prinsep MR, Caplan FR, Moore RE, Patterson GML, Honkanen RE, Boynton AL. Microcystin-LA from a blue-green alga belonging to the Stigonematales. Phytochemistry. 1992;31(4):1247-8.
8. Fiore MF, Genuário DB, da Silva CSP, Shishido TK, Moraes LAB, Neto RC, et al. Microcystin production by a freshwater spring cyanobacterium of the genus Fischerella. Toxicon. 2009;53(7-8):754-61.
9. Cirés S, Alvarez-Roa C, Wood SA, Puddick J, Loza V, Heimann K. First report of microcystin-producing Fischerella sp. (Stigonematales, Cyanobacteria) in tropical Australia. Toxicon. 2014;88:62-6.
10. Stratmann K, Burgoyne DL, Moore RE, Patterson GML, Smith CD. Hapalosin, a cyanobacterial cyclic depsipeptide with multidrug-resistance reversing activity. J Org Chem. 1994;59(24):7219-26.
11. Kim H, Krunic A, Lantvit D, Shen Q, Kroll DJ, Swanson SM, Orjala J: Nitrile-containing fischerindoles from the cultured cyanobacterium Fischerella sp. Tetrahedron 2012;68(15):3205-3209.
12. Coates RC, Podell S, Korobeynikov A, Lapidus A, Pevzner P, Sherman DH, et al. Characterization of cyanobacterial hydrocarbon composition and distribution of biosynthetic pathways. PLoS ONE. 2014;9(1), e85140.
13. Hagmann L, Jüttner F. Fischerellin A, a novel photosystem-II-inhibiting allelochemical of the cyanobacterium Fischerella muscicola with antifungal and herbicidal activity. Tetrahedron Lett. 1996;37(36):6539-42.
14. Gross EM, Wolk CP, Jüttner F. Fisherellin, a new allelochemical from the freshwater cyanoacterium Fischerlla muscicola. J Phycol. 1991;27(6):686-92.
15. Papke U, Gross EM, Francke W. Isolation, identification and determination of the absolute configuration of fischerellin B. A new algicide from the freshwater cyanobacterium Fischerella muscicola (Thuret). Tetrahedron Lett. 1997;38(3):379-82.
16. Prinsep MR, Moore RE, Levine IA, Patterson GML. Westiellamide, a bistratamide-related cyclic peptide from the blue-green alga Westiellopsis prolifica. J Nat Prod. 1992;55(1):140-2.
17. Falch BS, Koenig GM, Wright AD, Sticher O, Ruegger H, Bernardinelli G. Ambigol A and B: new biologically active polychlorinated aromatic compounds from the terrestrial blue-green alga Fischerella ambigua. J Org Chem. 1993;58(24):6570-5.
18. Wright AD, Papendorf O, König GM. Ambigol C and 2,4-dichlorobenzoic acid, natural products produced by the terrestrial cyanobacterium Fischerella ambigua. J Nat Prod. 2005;68(3):459-61.
19. Kang H-S, Krunic A, Orjala J. Stigonemapeptin, an Ahp-containing depsipeptide with elastase inhibitory activity from the bloom-forming freshwater cyanobacterium Stigonema sp. J Nat Prod. 2012;75(4):807-11.
20. Koodkaew I, Matsuyama S, Sunohara Y, Matsumoto H. Hapalocyclamide: a novel phytotoxic hexapeptide of the cyanobacterium Hapalosiphon sp. Tetrahedron Lett. 2012;53(8):977-9.
21. Ghasemi Y, Yazdi MT, Shafiee A, Amini M, Shokravi S, Zarrini G. Parsiguine, a novel antimicrobial substance from Fischerella ambigua. Pharm Biol. 2004;42(4-5):318-22.
22. Asthana R, Srivastava A, Kayastha A, Nath G, Singh S. Antibacterial potential of γ-linolenic acid from Fischerella sp. colonizing Neem tree bark. World J Microbiol Biotechnol. 2006;22(5):443-8.
23. Ehrenreich IM, Waterbury JB, Webb EA. Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes. Appl Environ Microbiol. 2005;71(11):7401-13.
24. Kehr J-C, Gatte Picchi D, Dittmann E. Natural product biosyntheses in cyanobacteria: A treasure trove of unique enzymes. Beilstein J Org Chem. 2011;7:1622-35.
25. Dittmann E, Neilan B, Börner T. Molecular biology of peptide and polyketide biosynthesis in cyanobacteria. Appl Microbiol Biotechnol. 2001;57(4):467-73.
26. Christiansen G, Dittmann E, Ordorika LV, Rippka R, Herdman M, Börner T. Nonribosomal peptide synthetase genes occur in most cyanobacterial genera as evidenced by their distribution in axenic strains of the PCC. Arch Microbiol. 2001;176(6):452-8.
27. Fischbach MA, Walsh CT. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem Rev. 2006;106(8):3468-96.
28. Liou GF, Khosla C. Building-block selectivity of polyketide synthases. Curr Opin Chem Biol. 2003;7(2):279-84.
29. Donadio S, Monciardini P, Sosio M. Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep. 2007;24(5):1073-109.
30. Cane DE, Walsh CT, Khosla C. Harnessing the biosynthetic code: Combinations, permutations, and mutations. Science. 1998;282(5386):63-8.
31. Walsh CT, Fischbach MA. Natural products version 2.0: Connecting genes to molecules. J Am Chem Soc. 2010;132(8):2469-93.
32. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep. 2013;30(1):108-60.
33. Sivonen K, Leikoski N, Fewer D, Jokela J. Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol. 2010;86(5):1213-25.
34. Wang H, Fewer DP, Sivonen K. Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS ONE. 2011;6(7), e22384.
35. Hemscheidt TK: Chapter two - microviridin biosynthesis. In: Methods Enzymol. Edited by David AH, vol. Volume 516: New York, Academic Press; 2012: 25-35.
36. Micallef ML, D'Agostino PM, Al-Sinawi B, Neilan BA, Moffitt MC. Exploring cyanobacterial genomes for natural product biosynthesis pathways. Mar Genomics. 2014.
37. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA. 2013;110(3):1053-8.
38. Calteau A, Fewer D, Latifi A, Coursin T, Laurent T, Jokela J, et al. Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria. BMC Genomics. 2014;15(1):977.
39. Hillwig ML, Fuhrman HA, Ittiamornkul K, Sevco TJ, Kwak DH, Liu X. Identification and characterization of a welwitindolinone alkaloid biosynthetic gene cluster in the stigonematalean cyanobacterium Hapalosiphon welwitschii. ChemBioChem. 2014;15(5):665-9.
40. Hillwig ML, Zhu Q, Liu X. Biosynthesis of ambiguine indole alkaloids in cyanobacterium Fischerella ambigua. ACS Chem Biol. 2013;9(2):372-7.
41. Micallef M, Sharma D, Bunn B, Gerwick L, Viswanathan R, Moffitt M. Comparative analysis of hapalindole, ambiguine and welwitindolinone gene clusters and reconstitution of indole-isonitrile biosynthesis from cyanobacteria. BMC Microbiol. 2014;14(1):1-18.
42. Gao Q, Garcia-Pichel F. An ATP-Grasp ligase involved in the last biosynthetic step of the iminomycosporine shinorine in Nostoc punctiforme ATCC 29133. J Bacteriol. 2011;193(21):5923-8.
43. Klähn S, Baumgartner D, Pfreundt U, Voigt K, Schoen V, Steglich C, et al. Alkane biosynthesis genes in cyanobacteria and their transcriptional organization. Front Bioeng Biotechnol. 2014;2.
44. Morin N, Vallaeys T, Hendrickx L, Natalie L, Wilmotte A. An efficient DNA isolation protocol for filamentous cyanobacteria of the genus Arthrospira. J Microbiol Methods. 2010;80(2):148-54.
45. Wilson K. Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K, editors. Current Protocols in Molecular Biology. New York: John Wiley & Sons, Inc; 2001.
46. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7(1):539.
47. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, et al. antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 2013;41(W1):W204-12.
48. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 2011;39(Database issue):D225-9.
49. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-10.
50. Bachmann BO, Ravel J: In silico prediction of microbial polyketide and nonribosomal peptide biosynthetic pathways from DNA sequence data. In: Methods Enzymol. Edited by David AH, vol. 458: New York, Academic Press; 2009: 181-217.
51. Röttig M, Medema MH, Blin K, Weber T, Rausch C, Kohlbacher O. NRPSpredictor2-a web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res. 2011;39 suppl 2:W362-7.
52. Ziemert N, Podell S, Penn K, Badger JH, Allen E, Jensen PR. The natural product domain seeker NaPDoS: a phylogeny based bioinformatic tool to classify secondary metabolite gene diversity. PLoS ONE. 2012;7(3), e34064.
53. Puigbo P, Wolf Y, Koonin E. Search for a 'Tree of Life' in the thicket of the phylogenetic forest. J Biol. 2009;8(6):59.
54. D'Agostino PM. Analysis of cyanobacterial genes for the biosynthesis of the anti-cancer compound hapalosin. University of Western Sydney. 2008.
55. Ramaswamy AV, Sorrels CM, Gerwick WH. Cloning and biochemical characterization of the hectochlorin biosynthetic gene cluster from the marine cyanobacterium Lyngbya majuscula. J Nat Prod. 2007;70(12):1977-86.
56. Edwards DJ, Marquez BL, Nogle LM, McPhail K, Goeger DE, Roberts MA, et al. Structure and biosynthesis of the jamaicamides, new mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscula. Chem Biol. 2004;11(6):817-33.
57. Fewer DP, Österholm J, Rouhiainen L, Jokela J, Wahlsten M, Sivonen K. Nostophycin biosynthesis is directed by a hybrid polyketide synthase-nonribosomal peptide synthetase in the toxic cyanobacterium Nostoc sp. strain 152. Appl Environ Microbiol. 2011;77(22):8034-40.
58. Magarvey NA, Beck ZQ, Golakoti T, Ding Y, Huber U, Hemscheidt TK, et al. Biosynthetic characterization and chemoenzymatic assembly of the cryptophycins. Potent anticancer agents from Nostoc cyanobionts. ACS Chem Biol. 2006;1(12):766-79.
59. Magarvey NA, Ehling-Schulz M, Walsh CT. Characterization of the cereulide NRPS aα-hydroxy acid specifying modules: activation of aα-keto acids and chiral reduction on the assembly line. J Am Chem Soc. 2006;128(33):10698-9.
60. Hackett JD, Wisecaver JH, Brosnahan ML, Kulis DM, Anderson DM, Bhattacharya D, et al. Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Mol Biol Evol. 2013;30(1):70-8.
61. Knauer SH, Hartl-Spiegelhauer O, Schwarzinger S, Hänzelmann P, Dobbek H. The Fe (II)/aα-ketoglutarate-dependent taurine dioxygenases from Pseudomonas putida and Escherichia coli are tetramers. FEBS J. 2012;279(5):816-31.
62. Ikeda H, Nonomiya T, Usami M, Ohta T, Omura S. Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis. Proc Nat Acad Sci. 1999;96(17):9509-14.
63. La Ferla B, Airoldi C, Zona C, Orsato A, Cardona F, Merlo S, et al. Natural glycoconjugates with antitumor activity. Nat Prod Rep. 2011;28(3):630-48.
64. Kersten RD, Ziemert N, Gonzalez DJ, Duggan BM, Nizet V, Dorrestein PC, et al. Glycogenomics as a mass spectrometry-guided genome-mining method for microbial glycosylated molecules. Proc Natl Acad Sci USA. 2013;110(47):E4407-16.
65. Kim EJ, Lee JH, Choi H, Pereira AR, Ban YH, Yoo YJ, et al. Heterologous production of 4-O-demethylbarbamide, a marine cyanobacterial natural product. Org Lett. 2012;14(23):5824-7.
66. Ongley SE, Bian X, Zhang Y, Chau R, Gerwick WH, Müller R, et al. High-titer heterologous production in E. coli of lyngbyatoxin, a protein kinase C activator from an uncultured marine cyanobacterium. ACS Chem Biol. 2013;8(9):1888-93.
67. Schmidt EW, Nelson JT, Rasko DA, Sudek S, Eisen JA, Haygood MG, et al. Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci USA. 2005;102(20):7315-20.
68. Donia MS, Ravel J, Schmidt EW. A global assembly line for cyanobactins. Nat Chem Biol. 2008;4(6):341-3.
69. Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB. Microbial biosynthesis of alkanes. Science. 2010;329(5991):559-62.
70. Agger SA, Lopez-Gallego F, Hoye TR, Schmidt-Dannert C. Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120. J Bacteriol. 2008;190(18):6084-96.
71. Giglio S, Jiang J, Saint CP, Cane DE, Monis PT. Isolation and characterization of the gene associated with geosmin production in cyanobacteria. Environ Sci Technol. 2008;42(21):8027-32.
72. Leikoski N, Liu L, Jokela J, Wahlsten M, Gugger M, Calteau A, et al. Genome mining expands the chemical diversity of the cyanobactin family to include highly modified linear peptides. Chem Biol. 2013;20(8):1033-43.
73. Donia M, Schmidt E: Cyanobactins-ubiquitous cyanobacterial ribosomal peptide metabolites, vol. 2: Elsevier: Oxford, UK; 2010.
74. Koehnke J, Bent A, Houssen WE, Zollman D, Morawitz F, Shirran S, et al. The mechanism of patellamide macrocyclization revealed by the characterization of the PatG macrocyclase domain. Nat Struct Mol Biol. 2012;19(8):767-72.
75. Banker R, Carmeli S. Tenuecyclamides A - D, cyclic hexapeptides from the cyanobacterium Nostoc spongiaeforme var. tenue. J Nat Prod. 1998;61(10):1248-51.
76. Schmidt EW, Donia MS: Chapter 23 Cyanobactin ribosomally synthesized peptides-A case of deep metagenome mining. In: Methods Enzymol. Edited by David AH, vol. 458: New York, Academic Press; 2009: 575-596.
77. Leikoski N, Fewer DP, Jokela J, Alakoski P, Wahlsten M, Sivonen K. Analysis of an inactive cyanobactin biosynthetic gene cluster leads to discovery of new natural products from strains of the genus Microcystis. PLoS ONE. 2012;7(8), e43002.
78. Ishitsuka MO, Kusumi T, Kakisawa H, Kaya K, Watanabe MM. Microviridin. A novel tricyclic depsipeptide from the toxic cyanobacterium Microcystis viridis. J Am Chem Soc. 1990;112(22):8180-2.
79. Shin HJ, Murakami M, Matsuda H, Yamaguchi K. Microviridins D-F, serine protease inhibitors from the cyanobacterium Oscillatoria agardhii (NIES-204). Tetrahedron. 1996;52(24):8159-68.
80. Philmus B, Christiansen G, Yoshida WY, Hemscheidt TK. Post-translational modification in microviridin biosynthesis. ChemBioChem. 2008;9(18):3066-73.
81. Philmus B, Guerrette JP, Hemscheidt TK. Substrate specificity and scope of MvdD, a GRASP-like ligase from the microviridin biosynthetic gene cluster. ACS Chem Biol. 2009;4(6):429-34.
82. Ziemert N, Ishida K, Liaimer A, Hertweck C, Dittmann E. Ribosomal synthesis of tricyclic depsipeptides in bloom-forming cyanobacteria. Angew Chem Int Edit. 2008;47(40):7756-9.
83. Oman TJ, van der Donk WA. Follow the leader: the use of leader peptides to guide natural product biosynthesis. Nat Chem Biol. 2010;6(1):9-18.
84. Havarstein LS, Diep DB, Nes IF. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol. 1995;16(2):229-40.
85. Willey JM, van der Donk WA. Lantibiotics: Peptides of diverse structure and function. Annu Rev Microbiol. 2007;61(1):477-501.
86. Goto Y, Li B, Claesen J, Shi Y, Bibb MJ, van der Donk WA. Discovery of unique lanthionine synthetases reveals new mechanistic and evolutionary insights. PLoS Biol. 2010;8(3), e1000339.
87. Haft D, Basu M, Mitchell D. Expansion of ribosomally produced natural products: a nitrile hydratase- and Nif11-related precursor family. BMC Biol. 2010;8(1):70.
88. Balskus EP, Walsh CT. The genetic and molecular basis for sunscreen biosynthesis in cyanobacteria. Science. 2010;329(5999):1653-6.
89. Rastogi RP, Incharoensakdi A. UV radiation-induced biosynthesis, stability and antioxidant activity of mycosporine-like amino acids (MAAs) in a unicellular cyanobacterium Gloeocapsa sp. CU2556. J Photochem Photobiol B: Biol. 2014;130:287-92.
90. Sinha RP, Ambasht NK, Sinha JP, Klisch M, Häder D-P. UV-B-induced synthesis of mycosporine-like amino acids in three strains of Nodularia (cyanobacteria). J Photochem Photobiol B: Biol. 2003;71(1-3):51-8.
91. Sorrels CM, Proteau PJ, Gerwick WH. Organization, evolution, and expression analysis of the biosynthetic gene cluster for scytonemin, a cyanobacterial UV-absorbing pigment. Appl Environ Microbiol. 2009;75(14):4861-9.
92. Soule T, Garcia-Pichel F, Stout V. Gene expression patterns associated with the biosynthesis of the sunscreen scytonemin in Nostoc punctiforme ATCC 29133 in response to UVA radiation. J Bacteriol. 2009;191(14):4639-46.
93. Englund E, Pattanaik B, Ubhayasekera SJK, Stensjö K, Bergquist J, Lindberg P. Production of squalene in Synechocystis sp. PCC 6803. PLoS ONE. 2014;9(3):e90270.
94. Donia MS, Hathaway BJ, Sudek S, Haygood MG, Rosovitz MJ, Ravel J, et al. Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians. Nat Chem Biol. 2006;2(12):729-35.
95. McIntosh JA, Lin Z, Tianero MDB, Schmidt EW. Aestuaramides, a natural library of cyanobactin cyclic peptides resulting from isoprene-derived claisen rearrangements. ACS Chem Biol. 2013;8(5):877-83.
96. Ziemert N, Ishida K, Quillardet P, Bouchier C, Hertweck C, de Marsac NT, et al. Microcyclamide biosynthesis in two strains of Microcystis aeruginosa: From structure to genes and vice versa. Appl Environ Microbiol. 2008;74(6):1791-7.