Abstract
Allosamidin, a typical secondary metabolite of Streptomyces, has been known as a chitinase inhibitor. We found that allosamidin can dramatically promote chitinase production and growth of its producer, Streptomyces sp. AJ9463, in a chitin medium at a few hundred nM. Allosamidin promoted production of the main chitinase detected in the culture filtrate and the chitin-hydrolytic activity of the chitinase was not inhibited by allosamidin at the concentration. The gene encoding the chitinase showed that it is a family 18 chitinase and it was revealed that two genes encoding proteins constructing two-component regulatory system were present at 5′-upstream region of the chitinase gene. Allosamidin is located in the microbial mycelia cultured in a medium without chitin, but it was released from the mycelia by responding to chitin. These results show that allosamidin acts as a key signal molecule for chitinase production in its producing strain, which may be useful for its growth in chitin-rich environment.
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Sakuda S, Isogai A, Matsumoto S, Suzuki A . Search for microbial insect growth regulators II. Allosamidin, a novel insect chitinase inhibitor. J Antibiot 40: 296–300 ( 1987)
Sakuda S, Isogai A, Matsumoto S, Suzuki A, Koseki K . Structure of allosamisin, a novel insect chitinase inhibitor, produced by Streptomyces sp. Tetrahedron Lett 27: 2475–2478 ( 1986)
Henrissat BA . Classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280: 309–316 ( 1991)
Sakuda S, Nishimoto Y, Ohi M, Watanabe M, Takayama S, Isogai A, Yamada Y . Effects of demethylallosamidin, a potent yeast chitinase inhibitor, on the cell division of yeast. Agric Biol Chem 54: 1333–1335 ( 1990)
Vinetz JM, Dave SK, Specht CA, Brameld KA, Xu B, Hayward R, Fidock DA . The chitinase pfCHT1 from the human malaria parasite Plasmodium faciparum lacks proenzyme and chitin-binding domains and displays unique substrate preferences. Proc Natl Acad Sci USA 96: 14061–14066 ( 1999)
Zhu Z, Zheng T, Homer RJ, Kim YK, Chen NY, Cohn L, Hamid Q, Elias JA . Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678–1682 ( 2004)
Nakanishi E, Okamoto S, Matsuura H, Nagasawa H, Sakuda S . Allosamidin, a chitinase inhibitor produced by Streptomyces, acts as an inducer of chitinase production in its producing strain. Proc Japan Academy B 77: 79–82 ( 2001)
Zhou Z, Sakuda S, Yamada Y . Biosynthetic studies on the chitinase inhibitor, allosamidin. Origin of the carbon and nitrogen atoms. J Chem Soc Perkin Trans I 1992: 1649–1652 ( 1992)
Kuranda MJ, Robbins PW . Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem 266: 19758–19767 ( 1991)
Kawachi R, Koike Y, Watanabe Y, Nishio T, Sakuda S, Nagasawa H, Oku T . Development of a genetic system in chitinase-producing Streptomyces and the application of an allosamidin-insensitive chitinase gene to homologous overexpression. Mol Biotechnol 26: 179–186 ( 2004)
Kawase T, Kanai R, Ohno T, Tanabe T, Nikaidou N, Miyashita K, Mitsutomi M, Watanabe T . Identification of three family 18 chitinase genes of Streptomyces griseus HUT6037. Chitin and Chitosan Research 7: 241–251 ( 2001)
Wang Q, Zhou Z, Sakuda S, Yamada Y . Purification of allosamidin-sensitive and -insensitive chitinases produced by allosamidin-producing Streptomyces. Biosci Biotechnol Biochem 57: 467–470 ( 1993)
Vetrivel KS, Pandian SK, Chaudhary U, Dharmalingam K . Purification, cloning, and DNA sequence analysis of a chitinase from an overproducing mutant of Streptomyces peucetius defective in daunorubicin biosynthesis. Can J Microbiol 47: 179–187 ( 2001)
Romaguera A, Menge U, Breves R, Diekmann H . Chitinases of Streptomyces olivaceoviridis and significance of processing for multiplicity. J Bacteriol 174: 3450–3454 ( 1992)
Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ . Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150: 2795–2806 ( 2004)
Tsujibo H, Hatano N, Okamoto T, Endo H, Miyamoto K, Inamori Y . Synthesis of chitinase in Streptomyces thermoviolaceus is regulated by a two-component sensor-regulator system. FEMS Microbiol Lett 181: 83–90 ( 1999)
Homerova D, Knirschova R, Kormanec J . Response regulator ChiR regulates expression of chitinase gene, chic, in Streptomyces coelicolor. Folia Microbiol 47: 499–505 ( 2002)
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Suzuki, S., Nakanishi, E., Ohira, T. et al. Chitinase Inhibitor Allosamidin Is a Signal Molecule for Chitinase Production in Its Producing Streptomyces. J Antibiot 59, 402–409 (2006). https://doi.org/10.1038/ja.2006.57
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DOI: https://doi.org/10.1038/ja.2006.57
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