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http://dx.doi.org/10.4014/jmb.1712.12014

Exogenous Indole Regulates Lipopeptide Biosynthesis in Antarctic Bacillus amyloliquefaciens Pc3  

Ding, Lianshuai (Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration)
Zhang, Song (Center for Proteomics, State Key Laboratory of Bio-Control, School of Life Science, Sun Yat-Sen University)
Guo, Wenbin (Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration)
Chen, Xinhua (Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration)
Publication Information
Journal of Microbiology and Biotechnology / v.28, no.5, 2018 , pp. 784-795 More about this Journal
Abstract
Bacillus amyloliquefaciens Pc3 was isolated from Antarctic seawater with antifungal activity. In order to investigate the metabolic regulation mechanism in the biosynthesis of lipopeptides in B. amyloliquefaciens Pc3, GC/MS-based metabolomics was used when exogenous indole was added. The intracellular metabolite profiles showed decreased asparagine, aspartic acid, glutamine, glutamic acid, threonine, valine, isoleucine, hexadecanoic acid, and octadecanoic acid in the indole-treated groups, which were involved in the biosynthesis of lipopeptides. B. amyloliquefaciens Pc3 exhibited a growth promotion, bacterial total protein increase, and lipopeptide biosynthesis inhibition upon the addition of indole. Besides this, real-time PCR analysis further revealed that the transcription of lipopeptide biosynthesis genes ituD, fenA, and srfA-A were downregulated by indole with 22.4-, 21.98-, and 26.0-fold, respectively. It therefore was speculated that as the metabolic flux of most of the amino acids and fatty acids were transferred to the synthesis of proteins and biomass, lipopeptide biosynthesis was weakened owing to the lack of precursor amino acids and fatty acids.
Keywords
Bacillus amyloliquefaciens; lipopeptides; metabolomics; metabolic flux;
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1 Ohno A, Ano T, Shoda M. 1995. Effect of temperature on production of lipopeptide antibiotics, iturin A and surfactin by a dual producer, Bacillus subtilis RB14, in solid-state fermentation. J. Ferment. Bioengineer. 80: 517-519.   DOI
2 Zhao J, Zhao P, Quan C, Jin L, Zheng W, Fan S. 2015. Comparative proteomic analysis of antagonistic Bacillus amyloliquefaciens Q-426 cultivated under different pH conditions. Biotechnol. Appl. Biochem. 62: 574-581.   DOI
3 Guez JS, Muller CH, Danze PM, Buchs J, Jacques P. 2008. Respiration activity monitoring system (RAMOS), an efficient tool to study the influence of the oxygen transfer rate on the synthesis of lipopeptide by Bacillus subtilis ATCC6633. J. Biotechnol. 134: 121-126.   DOI
4 Doroghazi JR, Albright JC. 2014. A roadmap for natural product discovery based on large-scale genomics and metabolomics. Nat. Chem. Biol. 10: 963-968.   DOI
5 Adu-Oppong B, Gasparrini AJ, Dantas G. 2017. Genomic and functional techniques to mine the microbiome for novel antimicrobials and antimicrobial resistance genes. Ann. NY Acad. Sci. 1388: 42-58.   DOI
6 Song C, Sundqvist G, Malm E, de Bruijn I, Kumar A, van de Mortel J, et al. 2015. Lipopeptide biosynthesis in Pseudomonas fluorescens is regulated by the protease complex ClpAP. BMC Microbiol. 15: 29.   DOI
7 Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR. 2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1: 387-396.   DOI
8 Peng B, Su YB, Li H, Han Y, Guo C, Tian YM, et al. 2015. Exogenous alanine and/or glucose plus kanamycin kills antibiotic-resistant bacteria. Cell Metab. 21: 249-261.   DOI
9 Fravel DR. 2005. Commercialization and implementation of biocontrol. Annu. Rev. Phytopathol. 43: 337-359.   DOI
10 Perez-Garcia A, Romero D, de Vicente A. 2011. Plant protection and growth stimulation by microorganisms: biotechnological applications of bacilli in agriculture. Curr. Opin. Biotechnol. 22: 187-193.   DOI
11 Berit E, Daniela Z, Alexander E, Ines F, Jürgen H, Annette N, et al. 2010. Metabolic profiling of Arabidopsis thaliana epidermal cells. J. Exp. Bot. 61: 1321.   DOI
12 Chen XH, Liu SR, Peng B, Li D, Cheng ZX, Zhu JX, et al. 2017. Exogenous L-valine promotes phagocytosis to kill multidrug-resistant bacterial pathogens. Front. Immunol. 8: 207.
13 Droby S, Wisniewski M, Macarisin D, Wilson C. 2009. Twenty years of postharvest biocontrol research: is it time for a new paradigm? Postharvest Biol. Technol. 52: 137-145.   DOI
14 Zeng ZH, Du CC, Liu SR, Li H, Peng XX, Peng B. 2017. Glucose enhances tilapia against Edwardsiella tarda infection through metabolome reprogramming. Fish Shellfish Immunol. 61: 34-43.   DOI
15 Li G, Young KD. 2013. Indole production by the tryptophanase TnaA in Escherichia coli is determined by the amount of exogenous tryptophan. Microbiology 159: 402-410.   DOI
16 Lee J-H, Lee J. 2010. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34: 426-444.   DOI
17 Wang Z, Li M, Peng B, Cheng Z, Li H, Peng X. 2016. GC- MS-based metabolome and metabolite regulation in serum- resistant Streptococcus agalactiae. J. Proteome Res. 15: 2246.   DOI
18 Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, et al. 2001. Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29.   DOI
19 Mukherjee S, Das P, Sen R. 2009. Rapid quantification of a microbial surfactant by a simple turbidometric method. J. Microbiol. Methods 76: 38-42.   DOI
20 Islam MT, Hashidoko Y, Deora A, Ito T, Tahara S. 2005. Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soilborne Peronosporomycetes. Appl. Environ. Microbiol. 71: 3786-3796.   DOI
21 Patterson GML, Bolis CM. 1997. Fungal cellwall polysaccharides elicit an antifungal secondary metabolite (phytoalexin) in the cyanobacterium Scytonema ocelutum2. J. Phycol. 33: 54-60.   DOI
22 Romero D, de Vicente A, Rakotoaly RH, Dufour SE, Veening JW, Arrebola E, et al. 2007. The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol. Plant Microbe Interact. 20: 430-440.   DOI
23 Stein T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56: 845-857.   DOI
24 Cochrane SA, Vederas JC. 2016. Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med. Res. Rev. 36: 4-31.   DOI
25 Lu H, Qian S, Muhammad U, Jiang X, Han J, Lu Z. 2016. Effect of fructose on promoting fengycin biosynthesis in Bacillus amyloliquefaciens fmb-60. J. Appl. Microbiol. 121: 1653-1664.   DOI
26 Yang H, Li X, Li X, Yu H, Shen Z. 2015. Identification of lipopeptide isoforms by MALDI-TOF-MS/MS based on the simultaneous purification of iturin, fengycin, and surfactin by RP-HPLC. Anal. Bioanal. Chem. 407: 2529-2542.   DOI
27 Cui P, Guo W, Chen X. 2017. Isotryptophan from Antarctic Bacillus amyloliquefaciens Pc3: purification, identification, characterization, and antifungal activity. Nat. Prod. Res. 31: 2153-2157.   DOI
28 Ongena M, Jacques P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16: 115-125.   DOI
29 Zhao H, Shao D, Jiang C, Shi J, Li Q, Huang Q, et al. 2017. Biological activity of lipopeptides from Bacillus. Appl. Microbiol. Biotechnol. 101: 5951-5960.   DOI
30 Jin H, Li K, Niu Y, Guo M, Hu C, Chen S, et al. 2015. Continuous enhancement of iturin A production by Bacillus subtilis with a stepwise two-stage glucose feeding strategy. BMC Biotechnol. 15: 53.   DOI
31 Montrone M, Oesterhelt D, Marwan W. 1996. Phosphorylation- independent bacterial chemoresponses correlate with changes in the cytoplasmic level of fumarate. J. Bacteriol. 178: 6882-6887.   DOI
32 Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: 2002-2007.
33 Besson F, Chevanet C, Michel G. 1987. Influence of the culture medium on the production of iturin A by Bacillus subtilis. J. Gen. Microbiol. 133: 767.
34 Aron ZD, Dorrestein PC, Blackhall JR, Kelleher NL, Walsh CT. 2005. Characterization of a new tailoring domain in polyketide biogenesis: the amine transferase domain of MycA in the mycosubtilin gene cluster. J. Am. Chem. Soc. 127: 14986.   DOI
35 Radwanski ER, Last RL. 1995. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7: 921-934.   DOI
36 Guo W, Cui P, Chen X. 2015. Complete genome of Bacillus sp. Pc3 isolated from the Antarctic seawater with antimicrobial activity. Mar. Genomics 20: 1-2.   DOI
37 Rao Q, Guo W, Chen X. 2015. Identification and characterization of an antifungal protein, AfAFPR9, produced by marine- derived Aspergillus fumigatus R9. J. Microbiol. Biotechnol. 25: 620-628.   DOI