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The YmdB protein regulates biofilm formation dependent on the repressor SinR in Bacillus cereus 0–9

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Abstract

YmdB, which can regulate biofilm formation independently, has been reported to exist in Bacillus subtilis. The B. cereus 0–9 genome also encodes a YmdB-like protein, which has measureable phosphodiesterase activity, and 72.35% sequence identity to YmdB protein of B. subtilis 168. In this work, we studied the function of YmdB protein and its encoding gene, ymdB, in B. cereus 0–9. Our results indicated that YmdB protein is critical for the biofilm formation of B. cereus 0–9. In ΔymdB mutant, the transcriptional levels of sinR and hag were up-regulated, and those of genes closely related to biofilm formation, such as sipW, tasA and calY, were down-regulated. Deletion of ymdB gene stimulates the swarming motility of B. cereus 0–9, and enhances it to travel outward, but reduces its ability to form complex spatial structures on the solid surface of MSgg plates. Hence, it is considered that YmdB plays a key role in biofilm formation, and this effect is likely achieved through the function of repressor SinR in B. cereus 0–9. Furthermore, by comparing the amino acid sequences of YmdB by Basic Local Alignment Search Tool (BLAST) in Genebank, we found that YmdB homologues are present in a variety of bacteria (Including Gram-negative bacteria) except B. subtilis and B. cereus. All these bacteria come at different evolutionary distances and belong to different genera. Therefore, we believe that YmdB exists in many types of bacteria and plays an important role in the stress-resistance of bacteria to adapt to the environment. These results can help us to further understand the biocontrol characteristics of B. cereus 0–9.

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References

  • Arnaud M, Chastanet A, Débarbouillé M (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive Bacteria. Appl Environ Microb 70:6887–6891

    Article  CAS  Google Scholar 

  • Branda SS, González-Pastor JE, Dervyn E et al (2004) Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186:3970–3979

    Article  CAS  Google Scholar 

  • Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98:11621–11626

    Article  CAS  Google Scholar 

  • Candela T, Fagerlund A, Buisson C et al (2019) CalY is a major virulence factor and a biofilm matrix protein. Mol Microbiol 111:1416–1429

    Article  CAS  Google Scholar 

  • Caro-Astorga J, Pérez-García A, De Vicente A, Romero D (2015) A genomic region involved in the formation of adhesin fibers in Bacillus cereus biofilms. Front Microbiol 5:1–11

    Article  Google Scholar 

  • Chu F, Kearns DB, Branda SS, Kolter R, Losick R (2006) Targets of the master regulator of biofilm formation in Bacillus subtilis. Mol Microbiol 59:1216–1228

    Article  CAS  Google Scholar 

  • Diethmaier C, Pietack N, Gunka K et al (2011) A novel factor controlling bistability in Bacillus subtilis: the YmdB protein affects flagellin expression and biofilm formation. J Bacteriol 193:5997–6007

    Article  CAS  Google Scholar 

  • Diethmaier C, Newman JA, Akos TK et al (2014) The YmdB phosphodiesterase is a global regulator of late adaptive responses in Bacillus subtilis. J bacteriol 196:265–275

    Article  Google Scholar 

  • Dubey G, Malli MG, Dubrovsky A, Amen T, Tsipshtein S, Rouvinski A (2016) Architecture and characteristics of bacterial nanotubes. Dev Cell 36:453–461

    Article  CAS  Google Scholar 

  • Fagerlund A, Dubois T, Økstad OA et al (2014) SinR control sentero toxin expression in Bacillus thuringiensis biofilms. PLoS ONE 9:e87532

    Article  Google Scholar 

  • Gao T, Li Y, Ding M, Chai Y, Wang Q (2017) The phosphotransferase system gene ptsI in Bacillus cereus regulates expression of sodA2 and contributes to colonization of wheat roots. Res Microbiol 168:524–535

    Article  CAS  Google Scholar 

  • Gao T, Ding M, Yang C, Fan H, Chai Y, Li Y (2019) The phosphotransferase system gene ptsH plays an important role in MnSOD production, biofilm formation, swarming motility, and root colonization in Bacillus cereus 905. Res Microbiol 170:86–96

    Article  CAS  Google Scholar 

  • Hobley L, Ostrowski A, Rao FV et al (2013) BslA is a self-assembling bacterial hydrophobin that coats the Bacillus subtilis biofilm. Proc Natl Acad Sci USA 110:13600–13605

    Article  CAS  Google Scholar 

  • Kang X, Wang L, Guo Y et al (2019) A comparative transcriptomic and proteomic analysis of hexaploid wheat’s responses to colonization by Bacillus velezensis and Gaeumannomyces graminis, both separately and combined. Mol Plant Microbe Interact 32:1336–1347

    Article  CAS  Google Scholar 

  • Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55:739–749

    Article  CAS  Google Scholar 

  • Kim T, Lee J, Kim K (2013) Escherichia coli YmdB regulates biofilm formation independently of its role as an RNase III modulator. BMC Microbiol 13:266

    Article  Google Scholar 

  • Kim M, Kim M, Kim K (2017) Ymdb-mediated down-regulation of sucA inhibits biofilm formation and induces apramycin susceptibility in Escherichia coli. Biochem Biophys Res Commun 483:252–257

    Article  CAS  Google Scholar 

  • Li M, Zhao J, Tang N, Sun H, Huang J (2018) Horizontal gene transfer from bacteria and plants to the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 9:701

    Article  Google Scholar 

  • Mäder U, Schmeisky AG, Flórez LA, Stülke J (2012) Subtiwiki—a comprehensive community resource for the model organism Bacillus subtilis. Nucleic Acids Res 40:D1278–1287

    Article  Google Scholar 

  • Mamou G, Malli MG, Rouvinski A, Rosenberg A, Ben-Yehuda S (2016) Early developmental program shapes colony morphology in bacteria. Cell Report 14:1850–1857

    Article  CAS  Google Scholar 

  • Majed R, Faille C, Kallassy M, Gohar M (2016) Bacillus cereus biofilms-same, only different. Front Microbiol 7:1054

    Article  Google Scholar 

  • Milton G, Draughn L, Bobay BG et al (2020) The solution structures and interaction of SinR and SinI: elucidating the mechanism of action of the master regulator switch for biofilm formation in Bacillus subtilis. J Mol Biol 432:343–357

    Article  CAS  Google Scholar 

  • Moons P, Chris M, Abram A (2009) Bacterial interactions in biofilms. Crit Rev Microbiol 35:157–168

    Article  CAS  Google Scholar 

  • Newman JA, Rodrigues C, Lewis RJ (2013) Molecular basis of the activity of SinR protein, the master regulator of biofilm formation in Bacillus subtilis. J Biol Chem 288:10766–10778

    Article  CAS  Google Scholar 

  • Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    Article  CAS  Google Scholar 

  • Pflughoeft KJ, Sumby P, Koehler TM (2011) Bacillus anthracis sin locus and regulation of secreted proteases. J Bacteriol 193:631–639

    Article  CAS  Google Scholar 

  • Romero D (2013) Bacterial determinants of the social behavior of Bacillus subtilis. Res Microbiol 164:788–798

    Article  Google Scholar 

  • Romero D, Vlamakis H, Losick R, Kolter R (2014) Functional analysis of the accessory protein TapA in Bacillus subtilis amyloid fiber assembly. J Bacteriol 196:1505–1513

    Article  Google Scholar 

  • Shin DH, Proudfoot M, Lim HJ, Choi IK, Kim SH (2007) Structural and enzymatic characterization of dr1281: a calcineurin-like phosphoesterase from Deinococcus radiodurans. Proteins 70:1000–1009

    Article  Google Scholar 

  • Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol 201:1121–1140

    Article  CAS  Google Scholar 

  • Stover AG, Driks A (1999a) Control of synthesis and secretion of the Bacillus subtilis protein YqxM. J Bacteriol 181:7065–7069

    Article  CAS  Google Scholar 

  • Stover AG, Driks A (1999b) Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. J Bacteriol 181:1664–1672

    Article  CAS  Google Scholar 

  • Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168

    Article  CAS  Google Scholar 

  • Wan T, Liu ZM, Li LF et al (2018) A genome for gnetophytes and early evolution of seed plants. Nat Plants 4:82–89

    Article  CAS  Google Scholar 

  • Xu Y, Chen M, Zhang Y et al (2014) The phosphotransferase system gene ptsI in the endophytic bacterium Bacillus cereus is required for biofilm formation, colonization, and biocontrol against wheat sharp eyespot. FEMS Microbiol Lett 354:142–152

    Article  CAS  Google Scholar 

  • Yan M, Wang X, Deng J et al (2016) DNA methylation and cerebellar development, the regulation of Notch and Shh pathway. Ital J Zool 83:34–42

    Article  CAS  Google Scholar 

  • Zhang J, Wang H, Huang Q et al (2020) Four superoxide dismutases of Bacillus cereus 0–9 are non-redundant and perform different functions in diverse living conditions. World J Microbiol Biotechnol 36:12

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by National Nature Science Foundation of China (NSFC) (31572047) and NSFC (31701831).

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  1. Juanmei Zhang and Haodong Wang have contributed equally to the work.

Authors and Affiliations

  1. Institute of Microbial Engineering, Hennan Univeristy, Kaifeng, 475004, Henan, People’s Republic of China

    Juanmei Zhang & Gang Wang

  2. School of Pharmaceutical, Hennan Univeristy, Kaifeng, 475004, Henan, People’s Republic of China

    Juanmei Zhang

  3. School of Life Sciences, Hennan Univeristy, Jinming Street, Kaifeng, 475004, Henan, People’s Republic of China

    Haodong Wang, Ting Xie, Qiubin Huang, Xi Xiong, Qing Liu & Gang Wang

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  1. Juanmei Zhang
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  2. Haodong Wang
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Correspondence to Gang Wang.

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Zhang, J., Wang, H., Xie, T. et al. The YmdB protein regulates biofilm formation dependent on the repressor SinR in Bacillus cereus 0–9. World J Microbiol Biotechnol 36, 165 (2020). https://doi.org/10.1007/s11274-020-02933-z

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