MsmR1, a Global Transcription Factor, Regulates Polymyxin Synthesis and Carbohydrate Metabolism in SC2

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2022 Dec 9

PMID 36483206

Authors

Dongying Zhao

Hui Li

Yanru Cui

Shengyue Tang

Chengqiang Wang

Binghai Du

Yanqin Ding

Affiliations

Soon will be listed here.

Abstract

The multiple-sugar metabolism regulator (MsmR), a transcription factor belonging to the AraC/XylS family, participates in polysaccharide metabolism and virulence. However, the transcriptional regulatory mechanisms of MsmR1 in remain unclear. In this study, knocking out was found to reduce polymyxin synthesis by the SC2-M1 strain. Chromatin immunoprecipitation assay with sequencing (ChIP-seq) revealed that most enriched pathway was that of carbohydrate metabolism. Additionally, electromobility shift assays (EMSA) confirmed the direct interaction between MsmR1 and the promoter regions of , , , , , , , and . MsmR1 stimulates polymyxin biosynthesis by directly binding to the promoter regions of and , while also directly regulating and influencing the citrate cycle (TCA cycle). In addition, MsmR1 directly activates and was beneficial for spore and biofilm formation. These results indicated that MsmR1 could regulate carbohydrate and amino acid metabolism, and indirectly affect biological processes such as polymyxin synthesis, biofilm formation, and motility. Moreover, MsmR1 could be autoregulated. Hence, this study expand the current knowledge of MsmR1 and will be beneficial for the application of SC2 in the biological control against the certain pathogens in pepper.

Citing Articles

Abh, AbrB3, and Spo0A play distinct regulatory roles during polymyxin synthesis in SC2.

Cui Y, Zhao D, Liu K, Mei X, Sun S, Du B Microbiol Spectr. 2023; 12(1):e0229323.

PMID: 38054717 PMC: 10782996. DOI: 10.1128/spectrum.02293-23.

References

Liu H, Li Y, Ge K, Du B, Liu K, Wang C . Interactional mechanisms of Paenibacillus polymyxa SC2 and pepper (Capsicum annuum L.) suggested by transcriptomics. BMC Microbiol. 2021; 21(1):70. PMC: 7931354. DOI: 10.1186/s12866-021-02132-2. View

Timmusk S, Grantcharova N, Wagner E . Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol. 2005; 71(11):7292-300. PMC: 1287669. DOI: 10.1128/AEM.71.11.7292-7300.2005. View

Mejia-Almonte C, Busby S, Wade J, van Helden J, Arkin A, Stormo G . Redefining fundamental concepts of transcription initiation in bacteria. Nat Rev Genet. 2020; 21(11):699-714. PMC: 7990032. DOI: 10.1038/s41576-020-0254-8. View

Sun D, Zhu J, Chen Z, Li J, Wen Y . SAV742, a Novel AraC-Family Regulator from Streptomyces avermitilis, Controls Avermectin Biosynthesis, Cell Growth and Development. Sci Rep. 2016; 6:36915. PMC: 5107987. DOI: 10.1038/srep36915. View

Russell R, Aduse-Opoku J, Sutcliffe I, Tao L, Ferretti J . A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J Biol Chem. 1992; 267(7):4631-7. View

Yu Z, Guo C, Qiu J . Precursor Amino Acids Inhibit Polymyxin E Biosynthesis in Paenibacillus polymyxa, Probably by Affecting the Expression of Polymyxin E Biosynthesis-Associated Genes. Biomed Res Int. 2015; 2015:690830. PMC: 4454717. DOI: 10.1155/2015/690830. View

Frandsen N, Stragier P . Plasmids for ectopic integration in Bacillus subtilis. Gene. 1996; 180(1-2):57-61. DOI: 10.1016/s0378-1119(96)00404-0. View

Nakata M, Podbielski A, Kreikemeyer B . MsmR, a specific positive regulator of the Streptococcus pyogenes FCT pathogenicity region and cytolysin-mediated translocation system genes. Mol Microbiol. 2005; 57(3):786-803. DOI: 10.1111/j.1365-2958.2005.04730.x. View

Slamti L, Lereclus D . The oligopeptide ABC-importers are essential communication channels in Gram-positive bacteria. Res Microbiol. 2019; 170(8):338-344. DOI: 10.1016/j.resmic.2019.07.004. View

10.

Zhang Q, Xing C, Kong X, Wang C, Chen X . ChIP-seq Analysis of the Global Regulator Vfr Reveals Novel Insights Into the Biocontrol Agent FD6. Front Microbiol. 2021; 12:667637. PMC: 8160232. DOI: 10.3389/fmicb.2021.667637. View

11.

Weber G, Klose K . The complexity of ToxT-dependent transcription in Vibrio cholerae. Indian J Med Res. 2011; 133:201-6. PMC: 3089052. View

12.

Perkins T, Davies M, Klemm E, Rowley G, Wileman T, James K . ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization. Mol Microbiol. 2012; 87(3):526-38. PMC: 3586657. DOI: 10.1111/mmi.12111. View

13.

Li H, Ding Y, Zhao J, Ge R, Qiu B, Yang X . Identification of a native promoter P for gene expression in Paenibacillus polymyxa. J Biotechnol. 2019; 295:19-27. DOI: 10.1016/j.jbiotec.2019.02.002. View

14.

Almengor A, McIver K . Transcriptional activation of sclA by Mga requires a distal binding site in Streptococcus pyogenes. J Bacteriol. 2004; 186(23):7847-57. PMC: 529090. DOI: 10.1128/JB.186.23.7847-7857.2004. View

15.

Dominguez-Cuevas P, Marin P, Marques S, Ramos J . XylS-Pm promoter interactions through two helix-turn-helix motifs: identifying XylS residues important for DNA binding and activation. J Mol Biol. 2007; 375(1):59-69. DOI: 10.1016/j.jmb.2007.10.047. View

16.

Solomon J, Su L, Shyn S, Grossman A . Isolation and characterization of mutants of the Bacillus subtilis oligopeptide permease with altered specificity of oligopeptide transport. J Bacteriol. 2003; 185(21):6425-33. PMC: 219414. DOI: 10.1128/JB.185.21.6425-6433.2003. View

17.

Warda A, Siezen R, Boekhorst J, Wells-Bennik M, de Jong A, Kuipers O . Linking Bacillus cereus Genotypes and Carbohydrate Utilization Capacity. PLoS One. 2016; 11(6):e0156796. PMC: 4896439. DOI: 10.1371/journal.pone.0156796. View

18.

Jeong H, Choi S, Ryu C, Park S . Chronicle of a Soil Bacterium: E681 as a Tiny Guardian of Plant and Human Health. Front Microbiol. 2019; 10:467. PMC: 6429003. DOI: 10.3389/fmicb.2019.00467. View

19.

Kavanagh K, Jornvall H, Persson B, Oppermann U . Medium- and short-chain dehydrogenase/reductase gene and protein families : the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci. 2008; 65(24):3895-906. PMC: 2792337. DOI: 10.1007/s00018-008-8588-y. View

20.

Chen X, Li P, Liu H, Chen X, Huang J, Luo C . A novel transcription factor UvCGBP1 regulates development and virulence of rice false smut fungus . Virulence. 2021; 12(1):1563-1579. PMC: 8344781. DOI: 10.1080/21505594.2021.1936768. View