Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Netzker, Tina ^a,b   Fischer, Juliane ^a,b   Weber, Jakob ^a,b   Mattern, Derek J ^a,b   König, Claudia C ^a,b   Valiante, Vito ^a   Schroeckh, Volker ^a   Brakhage, Axel A ^a,b  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Acetyltransferases; Aspergillus; Chromatin; Co culture; Gene cluster activation; Intermicrobial communication; Mass spectrometry; mixed fermentation; Natural products; Posttranslational histone modifications; Secondary metabolites; Streptomyces

Indexed keywords

HISTONE ACETYLTRANSFERASE;

ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; CELL INTERACTION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOTOXICITY; GENE ACTIVATION; GENE CLUSTER; GENE EXPRESSION; HISTONE MODIFICATION; MASS SPECTROMETRY; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; PARASITE CULTIVATION; REVIEW; SECONDARY METABOLISM; STREPTOMYCES; STREPTOMYCES RAPAMYCINICUS;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; BACTERIA (MICROORGANISMS); EMERICELLA NIDULANS; FUNGI; STREPTOMYCES;

EID: 84927130744     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00299     Document Type: Review

References (121)

1. AMINOV, R. I. 2009. The role of antibiotics and antibiotic resistance in nature. Environmental Microbiology, 11, 2970-2988.
2. ANDERSSON, D. I. & HUGHES, D. 2014. Microbiological effects of sublethal levels of antibiotics. Nat Rev Micro, 12, 465-478.
3. BAKER, S. P. & GRANT, P. A. 2007. The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene, 26, 5329-5340.
4. BBOSA, G. S., MWEBAZA, N., ODDA, J., KYEGOMBE, D. B. & NTALE, M. 2014. Antibiotics/antibacterial drug use, their marketing and promotion during the post- antibiotic golden age and their role in emergence of bacterial resistance. Health, 6, 410-425.
5. BERGMANN, S., SCHüMANN, J., SCHERLACH, K., LANGE, C., BRAKHAGE, A. A. & HERTWECK, C. 2007. Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat Chem Biol, 3, 213-217.
6. BERTRAND, S., AZZOLLINI, A., SCHUMPP, O., BOHNI, N., SCHRENZEL, J., MONOD, M., GINDRO, K. & WOLFENDER, J.-L. 2014a. Multi-well fungal co-culture for de novo metabolite-induction in time-series studies based on untargeted metabolomics. Molecular BioSystems, 10, 2289-2298.
7. BERTRAND, S., BOHNI, N., SCHNEE, S., SCHUMPP, O., GINDRO, K. & WOLFENDER, J.-L. 2014b. Metabolite induction via microorganism co-culture: A potential way to enhance chemical diversity for drug discovery. Biotechnology Advances, 32, 1180- 1204.
8. BERTRAND, S., SCHUMPP, O., BOHNI, N., BUJARD, A., AZZOLLINI, A., MONOD, M., GINDRO, K. & WOLFENDER, J.-L. 2013a. Detection of metabolite induction in fungal co-cultures on solid media by high-throughput differential ultra-high pressure liquid chromatography-time-of-flight mass spectrometry fingerprinting. Journal of Chromatography A, 1292, 219-228.
9. BERTRAND, S., SCHUMPP, O., BOHNI, N., MONOD, M., GINDRO, K. & WOLFENDER, J.-L. 2013b. De Novo Production of Metabolites by Fungal Co- culture of Trichophyton rubrum and Bionectria ochroleuca. Journal of Natural Products, 76, 1157-1165.
10. BODE, H. B., BETHE, B., HöFS, R. & ZEECK, A. 2002. Big Effects from Small Changes: Possible Ways to Explore Nature's Chemical Diversity. ChemBioChem, 3, 619-627.
11. BOK, J. W., CHIANG, Y.-M., SZEWCZYK, E., REYES-DOMINGUEZ, Y., DAVIDSON, A. D., SANCHEZ, J. F., LO, H.-C., WATANABE, K., STRAUSS, J., OAKLEY, B. R., WANG, C. C. C. & KELLER, N. P. 2009. Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol, 5, 462-464.
12. BOK, J. W. & KELLER, N. P. 2004. LaeA, a Regulator of Secondary Metabolism in Aspergillus spp. Eukaryotic Cell, 3, 527-535.
13. BOUIZGARNE, B. 2011. Bacteria for Plant Growth Promotion and Disease Management. Bacteria in Agrobiology: Plant Nutrient Management. Springer Science & Business Media.
14. BOUSLIMANI, A., SANCHEZ, L. M., GARG, N. & DORRESTEIN, P. C. 2014. Mass spectrometry of natural products: current, emerging and future technologies. Natural Product Reports, 31, 718-729.
15. BRADER, G., COMPANT, S. P., MITTER, B., TROGNITZ, F. & SESSITSCH, A. 2014. Metabolic potential of endophytic bacteria. Current Opinion in Biotechnology, 27, 30- 37.
16. BRAKHAGE, A. A. 2013. Regulation of fungal secondary metabolism. Nat Rev Micro, 11, 21-32.
17. BRAKHAGE, A. A., AL-ABDALLAH, Q., TUNCHER, A. & SPROTE, P. 2005. Evolution of beta-lactam biosynthesis genes and recruitment of trans-acting factors. Phytochemistry, 66, 1200-10.
18. BRAKHAGE, A. A., SCHUEMANN, J., BERGMANN, S., SCHERLACH, K., SCHROECKH, V. & HERTWECK, C. 2008. Activation of fungal silent gene clusters: A new avenue to drug discovery. In: PETERSEN, F. & AMSTUTZ, R. (eds.) Natural Compounds as Drugs. Birkhäuser Basel.
19. CARROZZA, M. J., UTLEY, R. T., WORKMAN, J. L. & CôTé, J. 2003. The diverse functions of histone acetyltransferase complexes. Trends in Genetics, 19, 321-329.
20. CHAPMAN & HALL. 2015. The Dictionary of Natural Products Online [Online]. CRC Press. Available: http://dnp.chemnetbase.com [Accessed 02.03.2015].
21. CHARLOP-POWERS, Z., OWEN, J. G., REDDY, B. V. B., TERNEI, M. A. & BRADY, S. F. 2014. Chemical-biogeographic survey of secondary metabolism in soil. Proceedings of the National Academy of Sciences, 111, 3757-3762.
22. CHEUNG, P., TANNER, K. G., CHEUNG, W. L., SASSONE-CORSI, P., DENU, J. M. & ALLIS, C. D. 2000. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell, 5, 905-15.
23. CHIANG, Y.-M., SZEWCZYK, E., NAYAK, T., DAVIDSON, A. D., SANCHEZ, J. F., LO, H.-C., HO, W.-Y., SIMITYAN, H., KUO, E., PRASEUTH, A., WATANABE, K., OAKLEY, B. R. & WANG, C. C. C. 2008. Molecular Genetic Mining of the Aspergillus Secondary Metabolome: Discovery of the Emericellamide Biosynthetic Pathway. Chemistry & Biology, 15, 527-532.
24. CHO, J. Y. & KIM, M. S. 2012. Induction of Antifouling Diterpene Production by Streptomyces cinnabarinus PK209 in Co-Culture with Marine-Derived Alteromonas sp. KNS-16. Bioscience, Biotechnology, and Biochemistry, 76, 1849-1854.
25. CHOOI, Y. H., FANG, J. X., LIU, H., FILLER, S. G., WANG, P. & TANG, Y. 2013. Genome Mining of a Prenylated and Immunosuppressive Polyketide from Pathogenic Fungi. Organic Letters, 15, 780-783.
26. CHUJO, T. & SCOTT, B. 2014. Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte-plant symbiosis. Molecular Microbiology, 92, 413-434.
27. CICHEWICZ, R. H. 2010. Epigenome manipulation as a pathway to new natural product scaffolds and their congeners. Natural Product Reports, 27, 11-22.
28. CORNETT, D. S., REYZER, M. L., CHAURAND, P. & CAPRIOLI, R. M. 2007. MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat Meth, 4, 828-833.
29. CRANEY, A., AHMED, S. & NODWELL, J. 2013. Towards a new science of secondary metabolism. J Antibiot, 66, 387-400.
30. CUETO, M., JENSEN, P. R., KAUFFMAN, C., FENICAL, W., LOBKOVSKY, E. & CLARDY, J. 2001. Pestalone, a New Antibiotic Produced by a Marine Fungus in Response to Bacterial Challenge. Journal of Natural Products, 64, 1444-1446.
31. DAVIES, J. 1990. What are antibiotics? Archaic functions for modern activities. Molecular Microbiology, 4, 1227-1232.
32. DEGENKOLB, T., HEINZE, S., SCHLEGEL, B., STROBEL, G., GR, AUML & FE, U. 2002. Formation of New Lipoaminopeptides, Acremostatins A, B, and C, by Co- cultivation of Acremonium sp. Tbp-5 and Mycogone rosea DSM 12973. Bioscience, Biotechnology, and Biochemistry, 66, 883-886.
33. DONIA, MOHAMED S., CIMERMANCIC, P., SCHULZE, CHRISTOPHER J., WIELAND BROWN, LAURA C., MARTIN, J., MITREVA, M., CLARDY, J., LININGTON, ROGER G. & FISCHBACH, MICHAEL A. 2014. A Systematic Analysis of Biosynthetic Gene Clusters in the Human Microbiome Reveals a Common Family of Antibiotics. Cell, 158, 1402-1414.
34. 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.
35. ESQUENAZI, E., YANG, Y.-L., WATROUS, J., GERWICK, W. H. & DORRESTEIN, P. C. 2009. Imaging mass spectrometry of natural products. Natural Product Reports, 26, 1521-1534.
36. FANG, J. & DORRESTEIN, P. C. 2014. Emerging mass spectrometry techniques for the direct analysis of microbial colonies. Current Opinion in Microbiology, 19, 120-129.
37. FREY-KLETT, P., BURLINSON, P., DEVEAU, A., BARRET, M., TARKKA, M. & SARNIGUET, A. 2011. Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists. Microbiology and Molecular Biology Reviews, 75, 583-609.
38. FRISVAD, J. C., RANK, C., NIELSEN, K. F. & LARSEN, T. O. 2009. Metabolomics of Aspergillus fumigatus. Medical Mycology, 47, S53-S71.
39. GACEK, A. & STRAUSS, J. 2012. The chromatin code of fungal secondary metabolite gene clusters. Applied Microbiology and Biotechnology, 95, 1389-1404.
40. GALáN, J.-C., GONZALEZ-CANDELAS, F., ROLAIN, J.-M. & CANTON, R. 2013. Antibiotics as selectors and accelerators of diversity in the mechanisms of resistance: From the resistome to genetic plasticity in the beta-lactamases world. Frontiers in Microbiology, 4.
41. GARCIA-GARCIA, J. C., BARAT, N. C., TREMBLEY, S. J. & DUMLER, J. S. 2009. Epigenetic Silencing of Host Cell Defense Genes Enhances Intracellular Survival of the Rickettsial Pathogen Anaplasma phagocytophilum. PLoS Pathog, 5, e1000488.
42. GEISER, D. M. 2009. Sexual structures in Aspergillus: morphology, importance and genomics. Medical Mycology, 47, S21-S26.
43. GOERS, L., FREEMONT, P. & POLIZZI, K. M. 2014. Co-culture systems and technologies: taking synthetic biology to the next level. J R Soc Interface, 11, 20140065.
44. GONZALEZ, D. J., HASTE, N. M., HOLLANDS, A., FLEMING, T. C., HAMBY, M., POGLIANO, K., NIZET, V. & DORRESTEIN, P. C. 2011. Microbial competition between Bacillus subtilis and Staphylococcus aureus monitored by imaging mass spectrometry. Microbiology, 157, 2485-2492.
45. GOVIND, C. K., ZHANG, F., QIU, H., HOFMEYER, K. & HINNEBUSCH, A. G. 2007. Gcn5 Promotes Acetylation, Eviction, and Methylation of Nucleosomes in Transcribed Coding Regions. Molecular Cell, 25, 31-42.
46. GRAUPNER, K., SCHERLACH, K., BRETSCHNEIDER, T., LACKNER, G., ROTH, M., GROSS, H. & HERTWECK, C. 2012. Imaging Mass Spectrometry and Genome Mining Reveal Highly Antifungal Virulence Factor of Mushroom Soft Rot Pathogen. Angewandte Chemie International Edition, 51, 13173-13177.
47. GROSS, J. 2014. Direct analysis in real time-a critical review on DART-MS. Analytical and Bioanalytical Chemistry, 406, 63-80.
48. HAMON, M. A., BATSCHé, E., RéGNAULT, B., THAM, T. N., SEVEAU, S., MUCHARDT, C. & COSSART, P. 2007. Histone modifications induced by a family of bacterial toxins. Proceedings of the National Academy of Sciences, 104, 13467- 13472.
49. HSU, C.-C. & DORRESTEIN, P. C. 2015. Visualizing life with ambient mass spectrometry. Current Opinion in Biotechnology, 31, 24-34.
50. HUFSKY, F., SCHEUBERT, K. & BOCKER, S. 2014. New kids on the block: novel informatics methods for natural product discovery. Natural Product Reports, 31, 807- 817.
51. KöNIG, C. C., SCHERLACH, K., SCHROECKH, V., HORN, F., NIETZSCHE, S., BRAKHAGE, A. A. & HERTWECK, C. 2013. Bacterium Induces Cryptic Meroterpenoid Pathway in the Pathogenic Fungus Aspergillus fumigatus. ChemBioChem, 14, 938-942.
52. KOURAKLIS, G. & THEOCHARIS, S. 2002. Histone Deacetylase Inhibitors and Anticancer Therapy. Current Medicinal Chemistry -Anti-Cancer Agents, 2, 477-484.
53. KUMBHAR, C., MUDLIAR, P., BHATIA, L., KSHIRSAGAR, A. & WATVE, M. 2014. Widespread predatory abilities in the genus Streptomyces. Archives of Microbiology, 196, 235-248.
54. LACKNER, G., MOEBIUS, N. & HERTWECK, C. 2011. Endofungal bacterium controls its host by an hrp type III secretion system. ISME J, 5, 252-261.
55. LEE, I., OH, J. H., SHWAB, E. K., DAGENAIS, T. R., ANDES, D. & KELLER, N. P. 2009. HdaA, a class 2 histone deacetylase of Aspergillus fumigatus, affects germination and secondary metabolite production. Fungal Genet Biol, 46, 782-90.
56. LEONE, M. R., LACKNER, G., SILIPO, A., LANZETTA, R., MOLINARO, A. & HERTWECK, C. 2010. An Unusual Galactofuranose Lipopolysaccharide That Ensures the Intracellular Survival of Toxin-Producing Bacteria in Their Fungal Host. Angewandte Chemie International Edition, 49, 7476-7480.
57. LI, C., WANG, J., LUO, C., DING, W. & COX, D. G. 2014. A new cyclopeptide with antifungal activity from the co-culture broth of two marine mangrove fungi. Natural Product Research, 28, 616-621.
58. LITZKA, O., PAPAGIANNOPOLOUS, P., DAVIS, M. A., HYNES, M. J. & BRAKHAGE, A. A. 1998. The penicillin regulator PENR1 of Aspergillus nidulans is a HAP-like transcriptional complex. European Journal of Biochemistry, 251, 758-767.
59. LIU, W.-T., YANG, Y.-L., XU, Y., LAMSA, A., HASTE, N. M., YANG, J. Y., NG, J., GONZALEZ, D., ELLERMEIER, C. D., STRAIGHT, P. D., PEVZNER, P. A., POGLIANO, J., NIZET, V., POGLIANO, K. & DORRESTEIN, P. C. 2010. Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proceedings of the National Academy of Sciences, 107, 16286-16290.
60. LUO, Y., COBB, R. E. & ZHAO, H. 2014. Recent advances in natural product discovery. Current Opinion in Biotechnology, 30, 230-237.
61. MAEKITA, T., NAKAZAWA, K., MIHARA, M., NAKAJIMA, T., YANAOKA, K., IGUCHI, M., ARII, K., KANEDA, A., TSUKAMOTO, T., TATEMATSU, M., TAMURA, G., SAITO, D., SUGIMURA, T., ICHINOSE, M. & USHIJIMA, T. 2006. High Levels of Aberrant DNA Methylation in Helicobacter pylori-Infected Gastric Mucosae and its Possible Association with Gastric Cancer Risk. Clin Cancer Res, 12, 989-995.
62. MARMANN, A., ALY, A., LIN, W., WANG, B. & PROKSCH, P. 2014. Co-Cultivation-A Powerful Emerging Tool for Enhancing the Chemical Diversity of Microorganisms. Marine Drugs, 12, 1043-1065.
63. MELIN, P., SCHNüRER, J. & WAGNER, E. 2002. Proteome analysis of Aspergillus nidulans reveals proteins associated with the response to the antibiotic concanamycin A, produced by Streptomyces species. Molecular Genetics and Genomics, 267, 695- 702.
64. MOEBIUS, N., ÜZüM, Z., DIJKSTERHUIS, J., LACKNER, G. & HERTWECK, C. 2014. Active invasion of bacteria into living fungal cells. eLife, 3, e03007.
65. MOODY, S. C. 2014. Microbial co-culture: harnessing intermicrobial signaling for the production of novel antimicrobials. Future Microbiology, 9, 575-578
66. MOREE, W. J., PHELAN, V. V., WU, C.-H., BANDEIRA, N., CORNETT, D. S., DUGGAN, B. M. & DORRESTEIN, P. C. 2012. Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proceedings of the National Academy of Sciences, 109, 13811-13816.
67. NATHAN, C. & CARS, O. 2014. Antibiotic Resistance - Problems, Progress, and Prospects. New England Journal of Medicine, 371, 1761-1763.
68. NüTZMANN, H.-W., FISCHER, J., SCHERLACH, K., HERTWECK, C. & BRAKHAGE, A. A. 2013. Distinct Amino Acids of Histone H3 Control Secondary Metabolism in Aspergillus nidulans. Applied and Environmental Microbiology, 79, 6102-6109.
69. NüTZMANN, H.-W., REYES-DOMINGUEZ, Y., SCHERLACH, K., SCHROECKH, V., HORN, F., GACEK, A., SCHüMANN, J., HERTWECK, C., STRAUSS, J. & BRAKHAGE, A. A. 2011. Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proceedings of the National Academy of Sciences, 108, 14282-14287.
70. OH, D.-C., JENSEN, P. R., KAUFFMAN, C. A. & FENICAL, W. 2005. Libertellenones A- D: Induction of cytotoxic diterpenoid biosynthesis by marine microbial competition. Bioorganic & Medicinal Chemistry, 13, 5267-5273.
71. OH, D.-C., KAUFFMAN, C. A., JENSEN, P. R. & FENICAL, W. 2007. Induced Production of Emericellamides A and B from the Marine-Derived Fungus Emericella sp. in Competing Co-culture. Journal of Natural Products, 70, 515-520.
72. OLA, A. R. B., THOMY, D., LAI, D., BRöTZ-OESTERHELT, H. & PROKSCH, P. 2013. Inducing Secondary Metabolite Production by the Endophytic Fungus Fusarium tricinctum through Coculture with Bacillus subtilis. Journal of Natural Products, 76, 2094-2099.
73. ONAKA, H., MORI, Y., IGARASHI, Y. & FURUMAI, T. 2011. Mycolic Acid-Containing Bacteria Induce Natural-Product Biosynthesis in Streptomyces Species. Applied and Environmental Microbiology, 77, 400-406.
74. PALMER, J. M., BOK, J. W., LEE, S., DAGENAIS, TAYLOR R. T., ANDES, D. R., KONTOYIANNIS, D. P. & KELLER, N. P. 2013. Loss of CclA, required for histone 3 lysine 4 methylation, decreases growth but increases secondary metabolite production in Aspergillus fumigatus. PeerJ, 1, e4.
75. PALMER, J. M., PERRIN, R. M., DAGENAIS, T. R. T. & KELLER, N. P. 2008. H3K9 Methylation Regulates Growth and Development in Aspergillus fumigatus. Eukaryotic Cell, 7, 2052-2060.
76. PARK, H. B., KWON, H. C., LEE, C.-H. & YANG, H. O. 2009. Glionitrin A, an Antibiotic- Antitumor Metabolite Derived from Competitive Interaction between Abandoned Mine Microbes. Journal of Natural Products, 72, 248-252.
77. PARTIDA-MARTINEZ, L. P., GROTH, I., SCHMITT, I., RICHTER, W., ROTH, M. & HERTWECK, C. 2007a. Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus. International Journal of Systematic and Evolutionary Microbiology, 57, 2583-2590.
78. PARTIDA-MARTINEZ, L. P. & HERTWECK, C. 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature, 437, 884-888.
79. PARTIDA-MARTINEZ, L. P. & HERTWECK, C. 2007. A Gene Cluster Encoding Rhizoxin Biosynthesis in "Burkholderia rhizoxina", the Bacterial Endosymbiont of the Fungus Rhizopus microsporus. ChemBioChem, 8, 41-45.
80. PARTIDA-MARTINEZ, L. P., MONAJEMBASHI, S., GREULICH, K.-O. & HERTWECK, C. 2007b. Endosymbiont-Dependent Host Reproduction Maintains Bacterial-Fungal Mutualism. Current Biology, 17, 773-777.
81. RANK, C., LARSEN, T. & FRISVAD, J. 2010. Functional systems biology of Aspergillus. In: MACHIDA, M. & GOMI, K. (eds.) Aspergillus: Molecular biology and Genomics. Wymondham, Norfolk, UK: Caister Academic Press.
82. RATEB, M. E., HALLYBURTON, I., HOUSSEN, W. E., BULL, A. T., GOODFELLOW, M., SANTHANAM, R., JASPARS, M. & EBEL, R. 2013. Induction of diverse secondary metabolites in Aspergillus fumigatus by microbial co-culture. RSC Advances, 3, 14444-14450.
83. REYES-DOMINGUEZ, Y., BOK, J. W., BERGER, H., SHWAB, E. K., BASHEER, A., GALLMETZER, A., SCAZZOCCHIO, C., KELLER, N. & STRAUSS, J. 2010. Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Molecular Microbiology, 76, 1376-1386.
84. ROLANDO, M., SANULLI, S., RUSNIOK, C., GOMEZ-VALERO, L., BERTHOLET, C., SAHR, T., MARGUERON, R. & BUCHRIESER, C. 2013. Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe, 13, 395-405.
85. ROSS, C., OPEL, V., SCHERLACH, K. & HERTWECK, C. 2014. Biosynthesis of antifungal and antibacterial polyketides by Burkholderia gladioli in coculture with Rhizopus microsporus. Mycoses, 57, 48-55.
86. ROZE, L. V., ARTHUR, A. E., HONG, S. Y., CHANDA, A. & LINZ, J. E. 2007. The initiation and pattern of spread of histone H4 acetylation parallel the order of transcriptional activation of genes in the aflatoxin cluster. Mol Microbiol, 66, 713-26.
87. ROZE, L. V., KOPTINA, A. V., LAIVENIEKS, M., BEAUDRY, R. M., JONES, D. A., KANARSKY, A. V. & LINZ, J. E. 2011. Willow volatiles influence growth, development, and secondary metabolism in Aspergillus parasiticus. Appl Microbiol Biotechnol, 92, 359-70.
88. SANCHEZ, J. F., SOMOZA, A. D., KELLER, N. P. & WANG, C. C. C. 2012. Advances in Aspergillus secondary metabolite research in the post-genomic era. Natural Product Reports, 29, 351-371.
89. SCHäBERLE, T., ORLAND, A. & KöNIG, G. 2014. Enhanced production of undecylprodigiosin in Streptomyces coelicolor by co-cultivation with the corallopyronin A-producing myxobacterium, Corallococcus coralloides. Biotechnology Letters, 36, 641-648.
90. SCHERLACH, K. & HERTWECK, C. 2009. Triggering cryptic natural product biosynthesis in microorganisms. Organic & Biomolecular Chemistry, 7, 1753-1760.
91. SCHERLACH, K., LACKNER, G., GRAUPNER, K., PIDOT, S., BRETSCHNEIDER, T. & HERTWECK, C. 2013. Biosynthesis and Mass Spectrometric Imaging of Tolaasin, the Virulence Factor of Brown Blotch Mushroom Disease. ChemBioChem, 14, 2439- 2443.
92. SCHERLACH, K., NüTZMANN, H.-W., SCHROECKH, V., DAHSE, H.-M., BRAKHAGE, A. A. & HERTWECK, C. 2011. Cytotoxic Pheofungins from an Engineered Fungus Impaired in Posttranslational Protein Modification. Angewandte Chemie International Edition, 50, 9843-9847.
93. SCHERLACH, K., PARTIDA-MARTINEZ, L. P., DAHSE, H.-M. & HERTWECK, C. 2006. Antimitotic Rhizoxin Derivatives from a Cultured Bacterial Endosymbiont of the Rice Pathogenic Fungus Rhizopus microsporus. Journal of the American Chemical Society, 128, 11529-11536.
94. SCHMITT, I., PARTIDA-MARTINEZ, L. P., WINKLER, R., VOIGT, K., EINAX, E., DOLZ, F., TELLE, S., WOSTEMEYER, J. & HERTWECK, C. 2008. Evolution of host resistance in a toxin-producing bacterial-fungal alliance. ISME J, 2, 632-641.
95. SCHROECKH, V., NüTZMANN, H.-W. & BRAKHAGE, A. A. 2014. Fungal-Actinomycete Interactions-Wakening of Silent Fungal Secondary Metabolism Gene Clusters via Interorganismic Interactions. Natural Products. John Wiley & Sons, Inc.
96. SCHROECKH, V., SCHERLACH, K., NüTZMANN, H.-W., SHELEST, E., SCHMIDT-HECK, W., SCHUEMANN, J., MARTIN, K., HERTWECK, C. & BRAKHAGE, A. A. 2009. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proceedings of the National Academy of Sciences, 106, 14558-14563.
97. SEYEDSAYAMDOST, M. R. & CLARDY, J. 2014. Natural products and synthetic biology. ACS Synth Biol, 3, 745-7.
98. SHAABAN, M. I., BOK, J. W., LAUER, C. & KELLER, N. P. 2010. Suppressor Mutagenesis Identifies a Velvet Complex Remediator of Aspergillus nidulans Secondary Metabolism. Eukaryotic Cell, 9, 1816-1824.
99. SHIH, C.-J., CHEN, P.-Y., LIAW, C.-C., LAI, Y.-M. & YANG, Y.-L. 2014. Bringing microbial interactions to light using imaging mass spectrometry. Natural Product Reports, 31, 739-755.
100. SHWAB, E. K., BOK, J. W., TRIBUS, M., GALEHR, J., GRAESSLE, S. & KELLER, N. P. 2007. Histone Deacetylase Activity Regulates Chemical Diversity in Aspergillus. Eukaryotic Cell, 6, 1656-1664.
101. SOUKUP, A. A., CHIANG, Y. M., BOK, J. W., REYES-DOMINGUEZ, Y., OAKLEY, B. R., WANG, C. C., STRAUSS, J. & KELLER, N. P. 2012. Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production. Mol Microbiol, 86, 314-30.
102. SOYER, J. L., EL GHALID, M., GLASER, N., OLLIVIER, B., LINGLIN, J., GRANDAUBERT, J., BALESDENT, M.-H., CONNOLLY, L. R., FREITAG, M., ROUXEL, T. & FUDAL, I. 2014. Epigenetic Control of Effector Gene Expression in the Plant Pathogenic Fungus Leptosphaeria maculans. PLoS Genet, 10, e1004227.
103. STOCKER-WORGOTTER, E. 2008. Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimatemetabolite production, and PKS genes. Natural Product Reports, 25, 188-200.
104. STRAHL, B. D. & ALLIS, C. D. 2000. The language of covalent histone modifications. Nature, 403, 41-45.
105. STRAND, M., CARLSSON, M., UVELL, H., ISLAM, K., EDLUND, K., CULLMAN, I., ALTERMARK, B., MEI, Y. F., ELOFSSON, M., WILLASSEN, N. P., WADELL, G. & ALMQVIST, F. 2014. Isolation and characterization of anti-adenoviral secondary metabolites from marine actinobacteria. Mar Drugs, 12, 799-821.
106. SUBRAMANI, R. & AALBERSBERG, W. 2012. Marine actinomycetes: An ongoing source of novel bioactive metabolites. Microbiological Research, 167, 571-580.
107. TARKKA, M., SARNIGUET, A. & FREY-KLETT, P. 2009. Inter-kingdom encounters: recent advances in molecular bacterium-fungus interactions. Current Genetics, 55, 233-243.
108. THEN BERGH, K. & BRAKHAGE, A. A. 1998. Regulation of the Aspergillus nidulans Penicillin Biosynthesis Gene acvA (pcbAB) by Amino Acids: Implication for Involvement of Transcription Factor PACC. Applied and Environmental Microbiology, 64, 843-849.
109. TILBURN, J., SARKAR, S., WIDDICK, D. A., ESPESO, E. A., OREJAS, M., MUNGROO, J., PENALVA, M. A. & ARST, H. N., JR. 1995. The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. Embo j, 14, 779-90.
110. TRAXLER, M. F., WATROUS, J. D., ALEXANDROV, T., DORRESTEIN, P. C. & KOLTER, R. 2013. Interspecies Interactions Stimulate Diversification of the Streptomyces coelicolor Secreted Metabolome. mBio, 4, e00459-13.
111. TRIBUS, M., GALEHR, J., TROJER, P., BROSCH, G., LOIDL, P., MARX, F., HAAS, H. & GRAESSLE, S. 2005. HdaA, a Major Class 2 Histone Deacetylase of Aspergillus nidulans, Affects Growth under Conditions of Oxidative Stress. Eukaryotic Cell, 4, 1736-1745.
112. TSUJI, N., KOBAYASHI, M., NAGASHIMA, K., WAKISAKA, Y. & KOIZUMI, K. 1976. A new antifungal antibiotic, trichostatin. J Antibiot (Tokyo), 29, 1-6.
113. WATANABE, T., IZAKI, K. & TAKAHASHI, H. 1982. New polyenic antibiotics active against gram-positive and -negative bacteria. I. Isolation and purification of antibiotics produced by Gluconobacter sp. W-315. J Antibiot (Tokyo), 35, 1141-7.
114. WATROUS, J., ROACH, P., HEATH, B., ALEXANDROV, T., LASKIN, J. & DORRESTEIN, P. C. 2013. Metabolic Profiling Directly from the Petri Dish Using Nanospray Desorption Electrospray Ionization Imaging Mass Spectrometry. Analytical Chemistry, 85, 10385-10391.
115. WATROUS, J. D. & DORRESTEIN, P. C. 2011. Imaging mass spectrometry in microbiology. Nat Rev Micro, 9, 683-694.
116. WHITT, J., SHIPLEY, S. M., NEWMAN, D. J. & ZUCK, K. M. 2014. Tetramic Acid Analogues Produced by Coculture of Saccharopolyspora erythraea with Fusarium pallidoroseum. Journal of Natural Products, 77, 173-177.
117. XU, Y., HE, H., SCHULZ, S., LIU, X., FUSETANI, N., XIONG, H., XIAO, X. & QIAN, P.- Y. 2010. Potent antifouling compounds produced by marine Streptomyces. Bioresource Technology, 101, 1331-1336.
118. YANG, Y.-L., XU, Y., STRAIGHT, P. & DORRESTEIN, P. C. 2009. Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol, 5, 885-887.
119. YU, J. H. & KELLER, N. 2005. Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol, 43, 437-58.
120. ZHU, F., CHEN, G., CHEN, X., HUANG, M. & WAN, X. 2011. Aspergicin, a new antibacterial alkaloid produced by mixed fermentation of two marine-derived mangrove epiphytic fungi. Chemistry of Natural Compounds, 47, 767-769.
121. ZUCK, K. M., SHIPLEY, S. & NEWMAN, D. J. 2011. Induced Production of N-Formyl Alkaloids from Aspergillus fumigatus by Co-culture with Streptomyces peucetius. Journal of Natural Products, 74, 1653-1657.