|
|
|
|
|
| Transcriptional profile of gene clusters involved in the methylerythritol phosphate pathway in Bacillus subtilis 916 |
XIAO Ya-jing1, 2*, GAO Tan-tan2*, PENG Qi2, ZHANG Jie2, SUN Dong-mei1, SONG Fu-ping2 |
1 College of Life Science and Technology, Heilongjiang Bayi Agricultural University, Daqing 163319, P.R.China
2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China |
|
|
|
|
Abstract The methylerythritol phosphate pathway is responsible for the biosynthesis of terpenoids, the largest class of secondary metabolites. Although the structures and functions of the proteins involved in this pathway have been well studied in Bacillus subtilis, only a few studies have reported the transcriptional profile of the genes involved. Therefore, we analyzed methylerythritol phosphate pathway genes in the genome of B. subtilis 916, which has been developed as a biological control agent against some rice diseases in China. Our results showed that methylerythritol phosphate pathway genes were distributed throughout the genome of this strain. These genes were transcribed during both the exponential and stationary phases. We further confirmed the transcription units of dxs, dxr, ispD, ispF, ipK, ispG, ispH, idi, and ispA in B. subtilis 916 through reverse transcription-PCR analyses; the results showed that these nine genes were located in seven different operons. The transcript start sites of the seven different operons were determined by 5´-rapid amplification of cDNA ends-PCR. Thus, our study provides a molecular basis at the transcriptional level for investigating homoterpene synthesis in the methylerythritol phosphate pathway of B. subtilis 916.
|
|
Received: 21 December 2017
Accepted:
|
| Fund: This work was supported by the National Natural Science Foundation of China (31530095). |
|
Corresponding Authors:
Correspondence SUN Dong-mei, Mobile: +86-13089069957, E-mail: sdmlzw@126.com; SONG Fu-ping, Tel: +86-10-62896634, E-mail: fpsong@ippcaas.cn
|
| About author: XIAO Ya-jing, Tel: +86-10-62815923, E-mail: 1565971446@qq.com; GAO Tan-tan, Tel: +86-10-62815923, E-mail: tantangao0537@gmail.com;
* These authors contributed equally to this study. |
Cite this article:
XIAO Ya-jing, GAO Tan-tan, PENG Qi, ZHANG Jie, SUN Dong-mei, SONG Fu-ping.
2019.
Transcriptional profile of gene clusters involved in the methylerythritol phosphate pathway in Bacillus subtilis 916. Journal of Integrative Agriculture, 18(3): 644-655.
|
Banerjee A, Sharkey T D. 2014. Methylerythritol 4-phosphate (MEP) pathway metabolic regulation. Natural Product Reports, 31, 1043–1055.
Bitok J K, Meyers C. 2012. 2C-Methyl-d-erythritol 4-phosphate enhances and sustains cyclodiphosphate synthase IspF activity. ACS Chemical Biology, 7, 1702–1710.
Boland W, Gäbler A, Gilbert M, Feng Z F. 1999. Biosynthesis of C11 and C16 homoterpenes in higher plants; stereochemistry of the C-C-bond cleavage reaction. ChemInform, 54, 14725–14736.
Brown A C, Eberl M, Crick D C, Jomaa H, Parish T. 2010. The nonmevalonate pathway of isoprenoid biosynthesis in Mycobacterium tuberculosis is essential and transcriptionally regulated by Dxs. Journal of Bacteriology, 192, 2424–2433.
Dick M, Sabelis M W, Takabayashi J, Bruin J, Posthumus M A. 1990. Plant strategies of manipulating predator prey interactions through allelochemicals: Prospects for application in pest control. Journal of Chemical Ecology, 16, 3091–3118.
Du L L, Qiu L L, Peng Q, Lereclus D, Zhang J, Song F P, Huang D F. 2012. Identification of the promoter in the intergenic region between orf1 and cry8Ea1 controlled by sigma H factor. Applied and Environmental Microbiology, 78, 4164–4168.
Evans R J, Davies D R, Bullard J M, Christensen J, Green L S, Guiles J W, Pata J D, Ribble W K, Janjic N, Jarvis T C. 2008. Structure of PolC reveals unique DNA binding and fidelity determinants. Proceedings of the National Academy of Sciences of the United States of America, 105, 20695–20700.
Frank A, Groll M. 2017. The methylerythritol phosphate pathway to isoprenoids. Chemical Reviews, 117, 5675–5703.
Giraud P, Créchet J B, Uzan M, Bontems F, Sizun C. 2015. Resonance assignment of the ribosome binding domain of E. coli ribosomal protein S1. Biomolecular NMR Assignments, 9, 107–111.
Guan Z, Xue D, Abdallah I I, Dijkshoorn L, Setroikromo R, Lv G Y, Quax W J. 2015. Metabolic engineering of Bacillus subtilis for terpenoid production. Applied Microbiology and Biotechnology, 99, 9395–9406.
Jin Y, Liu Z C, Li Y J, Liu W F, Tao Y, Wang G G. 2016. A structural and functional study on the 2-C-methyl-d-erythritol-4-phosphate cytidyltransferase (IspD) from Bacillus subtilis. Scientific Reports, 6, 36379.
Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Türbachova I, Eberl M, Zeidler J, Lichtenthaler H K, Soldati D, Beck E. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science, 285, 1573–1576.
Jung H, Liang J W, Jung Y, Lim D B. 2015. Characterization of cell death in Escherichia coli mediated by XseA, a large subunit of exonuclease VII. Journal of Microbiology, 53, 820–828.
Kuzma J, Nemecek-Marshall M, Pollock W H, Fall R. 1995. Bacteria produce the volatile hydrocarbon isoprene. Current Microbiology, 30, 97–103.
Kuzuyama T, Seto H. 2012. Two distinct pathways for essential metabolic precursors for isoprenoid biosynthesis. Proceedings of Japan Academy (Series B: Physical and Biological Sciences), 88, 41–52.
Lange B M, Rujan T, Martin W, Croteau R. 2000. Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes. Proceedings of the National Academy of Sciences of the United States of America, 97, 13172–13177.
Lee Y H, Helmann J D. 2013. Reducing the level of undecaprenyl pyrophosphate synthase has complex effects on susceptibility to cell wall antibiotics. Antimicrobial Agents and Chemotherapy, 57, 4267–4275.
Li F, Li W, Lin Y J, Pickett J A, Birkett M A, Wu K, Wang K, Wang G, Zhou J J. 2017. Expression of lima bean terpene synthases in rice enhances recruitment of a beneficial enemy of a major rice pest. Plant Cell and Environment, 41, 111–120.
Lois L M, Campos N, Putra S R, Danielsen K, Rohmer M, Boronat A. 1998. Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of d-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 95, 2105–2110.
Luo C P, Liu X H, Zhou H F, Wang X Y, Chen Z Y. 2015a. Nonribosomal peptide synthase gene clusters for lipopeptide biosynthesis in Bacillus subtilis 916 and their phenotypic functions. Applied and Environmental Microbiology, 81, 422–431.
Luo C P, Zhou H F, Zou J C, Wang X Y, Zhang R S, Xiang Y P, Chen Z Y. 2015b. Bacillomycin L. and surfactin contribute synergistically to the phenotypic features of Bacillus subtilis 916 and the biocontrol of rice sheath blight induced by Rhizoctonia solani. Applied Microbiology and Biotechnology, 99, 1897–1910.
Lv X M, Gu J L, Wang F, Xie W P, Liu M, Ye L D, Yu H W. 2016. Combinatorial pathway optimization in Escherichia coli by directed co-evolution of rate-limiting enzymes and modular pathway engineering. Biotechnology & Bioengineering, 113, 2661–2669.
Magalhães D M, Borges M, Laumann R, Woodcock C M, Pickett J A, Birkett M A, Blassioli-Moraes M. 2016. Influence of two acyclic homoterpenes (tetranorterpenes) on the foraging behavior of Anthonomus grandis Boh. Journal of Chemical Ecology, 42, 305–313.
Miller B, Heuser T, Zimmer W. 2000. Functional involvement of a deoxy-d-xylulose 5-phosphate reductoisomerase gene harboring locus of Synechococcus leopoliensis in isoprenoid biosynthesis. FEBS Letters, 481, 221–226.
Hess B M, Xue J, Markillie L M, Taylor R C, Wiley H S, Ahring B, Linggi B. 2013. Coregulation of terpenoid pathway genes and prediction of isoprene production in Bacillus subtilis using transcriptomics. PLoS ONE, 8, e66104.
Pelchat M, Lapointe L. 1999. In vivo and in vitro processing of the Bacillus subtilis transcript coding for glutamyl-tRNA synthetase, serine acetyltransferase, and cysteinyl-tRNA synthetase. RNA, 5, 281–289.
Rao G, Oldfield E. 2016. Structure and function of four classes of the 4Fe-4S protein, IspH. Biochemistry, 55, 4119–4129.
Richter A, Schaff C, Zhang Z W, Lipka A E, Tian F, Köllner T G, Schnee C, Preiß S, Irmisch S, Jander G, Boland W, Gershenzon J, Buckler E S, Degenhardt J. 2016. Characterization of biosynthetic pathways for the production of the volatile homoterpenes DMNT and TMTT in Zea mays. The Plant Cell, 28, 2651–2665.
Saggu G S, Garg S, Pala Z R, Yadav S K, Kochar S K, Kochar D K, Saxena V. 2017. Characterization of 4-hydroxy-3-methylbut-2-en-1-yl diphosphate synthase (IspG) from Plasmodium vivax and it’s potential as an antimalarial drug target. International Journal of Biological Macromolecules, 96, 466–473.
Sambrook B, Fritsch E, Maniatis T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
Song L S. 2003. Detection of farnesyl disphophate accumulation in yeast ERG9 mutants. Analytical Biochemistry, 317, 180–185.
Takahashi S, Kuzuyama T, Watanabe H, Seto H. 1998. A 1-deoxy-d-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-d-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 95, 9879–9884.
Tholl D, Sohrabi R, Huh J H, Lee S. 2011. The biochemistry of homoterpenes-common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry, 72, 1635–1646.
Wagner W, Helmig D, Fall R. 2000. Isoprene biosynthesis in Bacillus subtilis via the methylerythritol phosphate pathway. Journal of Natural Products, 63, 37–40.
Wang X Y, Luo C P, Chen Z Y. 2012. Genome sequence of the plant growth-promoting rhizobacterium Bacillus sp. strain 916. Journal of Bacteriology, 194, 5467–5468.
Wang G J, Zhang J, Song F P, Wu J, Feng S L, Huang D F. 2006. Engineered Bacillus thuringiensis GO33A with broad insecticidal activity against lepidopteran and coleopteran pests. Applied Microbiology and Biotechnology, 72, 924–930.
Wong F C, Beuning P J, Silvers C, Musier-Forsyth K. 2003. An isolated class II aminoacyl-tRNA synthetase insertion domain is functional in amino acid editing. The Journal of Biology Chemistry, 278, 52857–52864.
Xue D, Abdallah I I, de Haan I E, Sibbald M, Quax W. 2015. Enhanced C30 carotenoid production in Bacillus subtilis by systematic overexpression of MEP pathway genes. Applied Microbiology and Biotechnology, 99, 5907–5915.
Yang C, Gao X, Jiang Y, Sun B B, Gao F, Yang S. 2016. Synergy between methylerythritol phosphate pathway and mevalonate pathway for isoprene production in Escherichia coli. Metabolic Engineering, 37, 79–91.
Zhou G X, Wang X, Yan F, Wang X, Li R, Cheng J A, Lou Y G. 2011. Genome-wide transcriptional changes and defence-related chemical profiling of rice in response to infestation by the rice striped stem borer Chilo suppressalis. Physiologia Plantarum, 143, 21–40.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
