Journal of Microbiology

, Volume 56, Issue 4, pp 264–271 | Cite as

Identification of a novel phospholipase D gene and effects of carbon sources on its expression in Bacillus cereus ZY12

Microbial Physiology and Biochemistry

Abstract

In the present study, a new strain, Bacillus cereus ZY12, producing phospholipase D (PLD) was identified. The expression of PLD in this strain was found to be induced by its substrate, phosphatidylcholine (PC), and completely silenced by other carbon sources, such as glucose, fructose, and maltose, which are generally used in microbial growth cultures, thus presenting a unique expression pattern different from other PLD-producing microorganisms. This study is the first to report on the ability of B. cereus to produce PLD, and successfully clone its PLD-coding gene and identify its function, extending the knowledge on PLD distribution and evolution in microorganisms.

Keywords

Bacillus cereus phosphatidylcholine Phospholipase D substrate-induced gene expression 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12275_2018_7529_MOESM1_ESM.pdf (416 kb)
Supplementary material, approximately 415 KB.

References

  1. Choojit, S., Bornscheuer, U.T., Upaichit, A., and H-Kittikun, A. 2016. Efficient phosphatidylserine synthesis by a phospholipase D from Streptomyces sp. SC734 isolated from soil contaminated palm oil. Eur. J. Lipid Sci. Technol. 118, 803–813.Google Scholar
  2. Cole, R., Benns, G., and Proulx, P. 1974. Cardiolipin specific phospholipase D activity in Escherichia coli extracts. Biochim. Biophys. Acta 337, 325–332.CrossRefPubMedGoogle Scholar
  3. Comfurius, P. and Zwaal, R.F. 1977. The enzymatic synthesis of phosphatidylserine and purification by cm-cellulose column chromatography. Biochim. Biophys. Acta 488, 36–42.CrossRefPubMedGoogle Scholar
  4. Damnjanović, J., Kuroiwa, C., Tanaka, H., Ishida, K., Nakano, H., and Iwasaki, Y. 2016. Directing positional specificity in enzymatic synthesis of bioactive 1-phosphatidylinositol by protein engineering of a phospholipase D. Biotechnol. Bioeng. 113, 62–71.CrossRefPubMedGoogle Scholar
  5. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefPubMedGoogle Scholar
  6. Hagishita, T., Nishikawa, M., and Hatanaka, T. 2000. Isolation of phospholipase D producing microorganisms with high transphosphatidylation activity. Biotechnol. Lett. 22, 1587–1590.CrossRefGoogle Scholar
  7. Hodgson, A.L., Bird, P., and Nisbet, I.T. 1990. Cloning, nucleotide sequence, and expression in Escherichia coli of the phospholipase D gene from Corynebacterium pseudotuberculosis. J. Bacteriol. 172, 1256–1261.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Hu, F., Wang, H., Duan, Z.Q., and Yao, R.S. 2013. A novel phospholipase D constitutively secreted by Ochrobactrum sp. ASAG-PL1 capable of enzymatic synthesis of phosphatidylserine. Biotechnol. Lett. 35, 1317–1321.PubMedGoogle Scholar
  9. Jin, T. and Komagata, K. 1984. Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol. Lett. 25, 125–128.CrossRefGoogle Scholar
  10. Kim, O.S., Cho, Y.J., Lee, K., Yoon, S.H., Kim, M., Na, H., Park, S.C., Jeon, Y.S., Lee, J.H., Yi, H., et al., 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62, 716–721.CrossRefPubMedGoogle Scholar
  11. Lee, J.C. and Whang, K.S. 2015. Burkholderia humisilvae sp. nov., Burkholderia solisilvae sp. nov. and Burkholderia rhizosphaerae sp. nov. isolated from forest soil and rhizosphere soil. Int. J. Syst. Evol. Microbiol. 65, 2986–2992.CrossRefPubMedGoogle Scholar
  12. Li, B., Wang, J., Zhang, X.L., Zhao, B.X., and Niu, L. 2016. Aqueoussolid system for highly efficient and environmentally friendly transphosphatidylation catalyzed by phospholipase D to produce phosphatidylserine. J. Agric. Food Chem. 64, 1–30.CrossRefGoogle Scholar
  13. Liu, Y.H., Zhang, T., Qiao, J., Liu, X.G., Bo, J.X, Wang, J.L., and Lu, F.P. 2014. High-yield phosphatidylserine production via yeast surface display of phospholipase D from Streptomyces chromofuscus on Pichia pastoris. J. Agric. Food Chem. 62, 5354–5360.CrossRefPubMedGoogle Scholar
  14. Mao, X.Z., Liu, Q.Q., Qiu, Y.Q., Fan, X.Q., Han, Q.Q., Liu, Y.J., and Xue, C.H. 2017. Identification of a novel phospholipase D with high transphosphatidylation activity and its application in synthesis of phosphatidylserine and DHA-phosphatidylserine. J. Biotechnol. 249, 51–58.CrossRefPubMedGoogle Scholar
  15. Matsumoto, K. 1997. Phosphatidylserine synthase from bacteria. J. Biochim. Biophys. Acta 1348, 214–227.CrossRefGoogle Scholar
  16. McLain, N. and Dolan, J.W. 1997. Phospholipase D activity is required for dimorphic transition in Candida albicans. J. Microbiol. 143, 3521–3526.CrossRefGoogle Scholar
  17. Nakazawa, Y., Suzuki, R., Uchino, M., Sagane, Y., Kudo, T., Nagai, T., Sato, H., and Takano, K. 2010. Identification of actinomycetes producing phospholipase D with high transphosphatidylation activity. Curr. Microbiol. 60, 365–372.CrossRefPubMedGoogle Scholar
  18. Ono, Y. and White, D.C. 1970. Cardiolipin-specific phospholipase D activity in Haemophilus parainfluenzae. J. Bacteriol. 103, 111–115.PubMedPubMedCentralGoogle Scholar
  19. Pokorný, J. and Schmidt, S. 2011. Phospholipids, pp. 97–112. In Sikorski, Z.E. and Kolakowska, A. (eds.), Chemical, biological, and functional aspects of food lipids. CRC Press, Boca Raton, USA.Google Scholar
  20. Procyk, K.J., Kovarik, P., Von, G.A., and Baccarini, M. 1999. Salmonella typhimurium and lipopolysaccharide stimulate extracellularly regulated kinase activation in macrophages by a mechanism involving phosphatidylinositol 3-kinase and phospholipase D as novel intermediates. Infect. Immun. 67, 1011–1017.PubMedPubMedCentralGoogle Scholar
  21. Ramón, A., Señorale-Pose, M., and Marín, M. 2014. Inclusion bodies: not that bad Front. Microbiol. 5, 56.Google Scholar
  22. Saitou, N. and Nei, M. 1987. The neighbor-joining method-a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.PubMedGoogle Scholar
  23. Salzberg, L.I. and Helmann, J.D. 2008. Phenotypic and transcriptomic characterization of Bacillus subtilis mutants with grossly altered membrane composition. J. Bacteriol. 190, 7797–7807.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Shimbo, K., Yano, H., and Miyamoto, Y. 2014. Two Streptomyces strains that produce phospholipase D with high transphosphatidylation activity. Agric. Biol. Chem. 53, 3083–3085.Google Scholar
  25. Tamura, Y., Harada, Y., Nishikawa, S., Yamano, K., Kamiya, M., and Shiota, T. 2013. Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria. Cell Metab. 17, 709–718.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Tarfarosh, S.F.A., Tromboo, U., and Bhat, F. 2017. Search for a perfect Nootropic supplement combination-Can we increase human intelligence by nutritional supplements? J. Pharmacogn. Phytochem. 6, 1020–1024.Google Scholar
  28. Tong, C., Liu, L., Waters, D.L.E., and Bao, J.S. 2016. Association mapping and marker development of genes for starch lysophospholipid synthesis in rice. Rice Science 23, 287–296.CrossRefGoogle Scholar
  29. Uhm, T.B., Li, T., Bao, J., Chung, G., and Ryu, D.D.Y. 2005. Analysis of phospholipase D gene from Streptoverticillium reticulum, and the effect of biochemical properties of substrates on phospholipase D activity. Enzyme Microb. Technol. 37, 641–647.CrossRefGoogle Scholar
  30. Vakhapova, V., Cohen, T., Richter, Y., Herzog, Y., Kam, Y., and Korczyn, A.D. 2014. Phosphatidylserine containing omega-3 fatty acids may improve memory abilities in nondemented elderly individuals with memory complaints: results from an open-label extension study. Dement. Geriatr. Cogn. Disord. 38, 39–45.CrossRefPubMedGoogle Scholar
  31. Wilderman, P.J., Vasil, A.I., Johnson, Z., and Vasil, M.L. 2001. Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol. Microbiol. 39, 291–303.CrossRefPubMedGoogle Scholar
  32. Zambonelli, C., Morandi, P., Vanoni, M.A., Tedeschi, G., Servic, S., and Curti, B. 2003. Cloning and expression in Escherichia coli of the gene encoding Streptomyces PMF PLD, a phospholipase D with high transphosphatidylation activity. Enzyme Microb. Technol. 33, 676–688.CrossRefGoogle Scholar
  33. Zhang, Y.N., Lu, F.P., Chen, G.Q., Li, Y., and Wang, J.L. 2008. Expression, purification, and characterization of phosphatidylserine synthase from Escherichia coli K12 in Bacillus subtilis. J. Agric. Food Chem. 57, 122–126.CrossRefGoogle Scholar
  34. Zhao, Z.W., Yang, T.K., and Mu, Y. 2010. Fermentation conditions of phospholipase D production by Streptomyces chromofuscus. China Oils Fats 35, 52–57.Google Scholar
  35. Zhou, W.B., Gong, J.S., Hou, H.J., Li, H., Lu, Z.M., Xu, H.Y., Xu, Z.H., and Shi, J.S. 2017. Mining of a phospholipase D and its application in enzymatic preparation of phosphatidylserine. Bioengineered 9, 80–89.CrossRefPubMedGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological EngineeringDalian Polytechnic UniversityDalianP. R. China
  2. 2.School of Food and Biological EngineeringQiqihar UniversityQiqiharP. R. China

Personalised recommendations