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Lipidomics characterization of the alterations of Trichoderma brevicompactum membrane glycerophospholipids during the fermentation phase

  • Yunfan Bai
  • Yuran Gao
  • Xin Lu
  • Huiyu WangEmail author
Metabolic Engineering and Synthetic Biology - Original Paper

Abstract

The biological membrane lipid composition has been demonstrated to greatly influence the secretion of secondary metabolites. This study was conducted to investigate the periodical alterations of whole cellular lipids and their associations with secondary products in Trichoderma brevicompactum. An electrospray ionization–mass spectrometry-based lipidomics strategy was used to acquire the metabolic profiles of membrane lipids during fermentation. Univariate analyses showed that most fungi glycerophospholipids were significantly altered at the early phase compared with the late phase. In addition, correlation analyses showed high correlations between phosphatidylcholine alterations and fermentation duration. In addition, the fermentation-associated alterations of phosphatidylcholines were found to be in accordance with the degrees of unsaturation of acyl-chains. Harzianum A reached a maximum on the 12th day, while trichodermin and 6-pentyl-2H-pyran-2-one showed the highest abundances on the 9th day, both of which were inclined to correlate with the alterations of phosphatidylcholines and phosphatidylethanolamines, respectively. These findings demonstrated that the alterations of the membrane lipid species in Trichoderma spp. were associated with the fermentation phases and might influence the secretion of specific secondary products, which may be useful in studying the optimization of secondary products in Trichoderma spp.

Keywords

Trichoderma brevicompactum Metabolic profile Lipidomics Secondary product Glycerophospholipid 

Notes

Acknowledgements

This study was funded by the Science and Technology Project of Qiqihar City (SFGG-201543) and the Doctoral Scientific Fund Project (QY2015B-03). We sincerely express our appreciation to the Forest Department in Northeast Forest University for donating the Trichoderma brevicompactum strain to this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10295_2019_2152_MOESM1_ESM.tif (8.3 mb)
Fig. S1 Score plot of PCA model constructed with 128 lipid species in T. brevicompactum mycelia. Black, red, green, blue, yellow boxes indicate T. brevicompactum mycelia collected on the 3rd day, the 6th day, the 9th day, the 12th day, and the 15th day, respectively
10295_2019_2152_MOESM2_ESM.tif (8 mb)
Fig. S2 Corresponding validation plot of PLS-DA model. Green dots are R2 values, while blue dots are Q2 values
10295_2019_2152_MOESM3_ESM.tif (5.6 mb)
Fig. S3 DVCs constructed with PEs and PSs. (a) DVC of PEs; (b) DVCs of PSs. Colors and sizes of dots mean different degrees of fold-change
10295_2019_2152_MOESM4_ESM.tif (7.9 mb)
Fig. S4 Spearman correlation analyses between PCs, PEs, PSs and (a) 6-Pentyl-2H-pyran-2-one; (b) harzianum A; (c) trichodermin. Green, yellow, and purple dots indicate PC, PE, PS lipid species, respectively. Red dots indicate the means of correlation coefficients
10295_2019_2152_MOESM5_ESM.tif (3.7 mb)
Fig. S5 Spearman correlation analyses between growth phases and (a) different lipid categories (PC, PE, PS). The numbers of lipid species with correlation coefficients > 0.8 represented. Purple, red, pink, blue, green represent LPCs, LPEs, PCs, PEs, and PSs, respectively; (b) three secondary metabolites (trichoderma, harzianum A, 6-pentyl pyrone). The correlation coefficients were shown in the table
10295_2019_2152_MOESM6_ESM.doc (296 kb)
Table S1 Basic information of 128 lipid species in T. brevicompactum mycelia

References

  1. 1.
    Alexandre H, Rousseaux I, Charpentier C (1994) Relationship between ethanol tolerance, lipid composition and plasma membrane fluidity in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiol Immunol 124:17–22.  https://doi.org/10.1111/j.1574-6968.1994.tb07255.x CrossRefGoogle Scholar
  2. 2.
    Bailey MJ, Tahtiharju J (2003) Efficient cellulase production by Trichoderma reesei in continuous cultivation on lactose medium with a computer-controlled feeding strategy. Appl Microbiol Biotechnol 62:156–162.  https://doi.org/10.1007/s00253-003-1276-9 CrossRefPubMedGoogle Scholar
  3. 3.
    Benítez T, Rincón AM, Limón MC et al (2005) Biocontrol mechanism of Trichoderma strains. Int Microbiol 7(4):249–260Google Scholar
  4. 4.
    Bernat P, Gajewska E, Szewczyk R et al (2014) Tributyltin (TBT) induces oxidative stress and modifies lipid profile in the filamentous fungus Cunninghamella elegans. Environ Sci Pollut Res Int 21:4228–4235.  https://doi.org/10.1007/s11356-013-2375-5 CrossRefPubMedGoogle Scholar
  5. 5.
    Boeszebattaglia K, Schimmel R (1997) Cell membrane lipid composition and distribution: implications for cell function and lessons learned from photoreceptors and platelets. J Exp Biol 200(Pt 23):2927.  https://doi.org/10.1016/s0006-3495(02)75223-5 Google Scholar
  6. 6.
    Carrasco L, Barbacid M, Vazquez D (1973) The trichodermin group of antibiotics, inhibitors of peptide bond formation by eukaryotic ribosomes. Bba 312(2):368–376.  https://doi.org/10.1016/0005-2787(73)90381-x PubMedGoogle Scholar
  7. 7.
    Classen JJ, Engler CR, Kenerley CM, Whittaker AD (2000) A logistic model of subsurface fungal growth with application to bioremediation. J Environ Sci Health A Tox Hazard Subst Environ Eng 35:465–488.  https://doi.org/10.1080/10934520009376982 CrossRefGoogle Scholar
  8. 8.
    Cooney JM, Lauren DR et al (1997) Effect of solid substrate, liquid supplement, and harvest time on 6-n-Pentyl-2H-pyran-2-one (6PAP) Production by Trichoderma spp. J Agric Food Chem 45(2):531–534.  https://doi.org/10.1021/jf960473i CrossRefGoogle Scholar
  9. 9.
    Corley DG, Millerwideman M, Durley RC (1994) Isolation and structure of harzianum A: a new trichothecene from trichoderma harzianum. J Nat Prod 57(3):422–425.  https://doi.org/10.1021/np50105a019 CrossRefPubMedGoogle Scholar
  10. 10.
    Dennis EA (2009) Lipidomics joins the omics evolution. Proc Natl Acad Sci U S A 106(7):2089–2090.  https://doi.org/10.1073/pnas.0812636106 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Gao Q, Lu Y, Yao H et al (2016) Phospholipid homeostasis maintains cell polarity, development and virulence in metarhizium robertsii. Environ Microbiol 18:3976–3990.  https://doi.org/10.1111/1462-2920.13408 CrossRefPubMedGoogle Scholar
  12. 12.
    Harman GE, Howell CR, Viterbo A et al (2004) Trichoderma species–opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56.  https://doi.org/10.1038/nrmicro797 CrossRefPubMedGoogle Scholar
  13. 13.
    Hishikawa D, Hashidate T, Shimizu T et al (2014) Diversity and function of membrane glycerophospholipids generated by the remodeling pathway in mammalian cells. J Lipid Res 55(5):799.  https://doi.org/10.1194/jlr.R046094 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Hishikawa D, Valentine WJ, Hishikawa YL, Shindou H, Shimizu T (2017) Metabolism and functions of docosahexaenoic acid-containing membrane glycerophospholipids. FEBS Lett 591:2730–2744.  https://doi.org/10.1002/1873-3468.12825 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Jeleń H, Błaszczyk L, Chełkowski J et al (2013) Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycol Prog 13(3):589–600.  https://doi.org/10.1007/s11557-013-0942-2 Google Scholar
  16. 16.
    Kabelitz N, Santos PM, Heipieper HJ (2003) Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus. FEMS Microbiol Lett 220:223–227.  https://doi.org/10.1016/s0378-1097(03)00103-4 CrossRefPubMedGoogle Scholar
  17. 17.
    Kilpinen L, Sahle FT, Oja S et al (2013) Aging bone marrow mesenchymal stromal cells have altered membrane glycerophospholipid composition and functionality. J Lipid Res 54:622–635.  https://doi.org/10.1194/jlr.M030650 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Lattif AA, Mukherjee PK, Chandra J, Roth MR, Welti R, Rouabhia M, Ghannoum MA (2011) Lipidomics of Candida albicans biofilms reveals phase-dependent production of phospholipid molecular classes and role for lipid rafts in biofilm formation. Microbiology 157:3232–3242.  https://doi.org/10.1099/mic.0.051086-0 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Meer GV, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124.  https://doi.org/10.1038/nrm2330 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Monte E (2001) Understanding Trichoderma: between biotechnology and microbial ecology. Int Microbiol 4:1–4.  https://doi.org/10.1007/s101230100001 PubMedGoogle Scholar
  21. 21.
    Mukherjee PK, Horwitz BA, Kenerley CM (2012) Secondary metabolism in Trichoderma—a genomic perspective. MBio 158:35–45.  https://doi.org/10.1099/mic.0.053629-0 Google Scholar
  22. 22.
    Nielsen KF, Fenhan TG, Zafari D et al (2005) Trichothecene Production by Trichoderma brevicompactum. J Agric Food Chem 53(21):8190.  https://doi.org/10.1021/jf051279b CrossRefPubMedGoogle Scholar
  23. 23.
    Oda S, Isshiki K, Ohashi S (2009) Production of 6-pentyl-α-pyrone with Trichoderma atroviride and its mutant in a novel extractive liquid-surface immobilization (Ext-LSI) system. Process Biochem 44:625–630.  https://doi.org/10.1016/j.procbio.2009.01.017 CrossRefGoogle Scholar
  24. 24.
    Rainville PD, Stumpf CL, Shockcor JP et al (2007) Novel application of reversed-phase UPLC-oaTOF-MS for lipid analysis in complex biological mixtures: a new tool for lipidomics. J Proteome Res 6(2):552–558.  https://doi.org/10.1021/pr060611b CrossRefPubMedGoogle Scholar
  25. 25.
    Rawicz W, Olbrich KC, McIntosh T et al (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79(1):328–339.  https://doi.org/10.1016/s0006-3495(00)76295-3 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Szule JA, Fuller NL, Rand RP (2002) The effects of acyl chain length and saturation of diacylglycerols and phosphatidylcholines on membrane monolayer curvature. Biophys J 83(2):977–984.  https://doi.org/10.1016/s0006-3495(02)75223-5 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Tarus PK, Lang’Atthoruwa CC, Wanyonyi AW et al (2003) Bioactive metabolites from Trichoderma harzianum and Trichoderma longibrachiatum. Bull Chem Soc Ethiop 17(2):185–190Google Scholar
  28. 28.
    Tijerino A, Hermosa R, Cardoza RE et al (2011) Overexpression of the Trichoderma brevicompactum tri5 gene: effect on the expression of the trichodermin biosynthetic genes and on tomato seedlings. Toxins (Basel) 3:1220–1232.  https://doi.org/10.3390/toxins3091220 CrossRefGoogle Scholar
  29. 29.
    Turk M, Mejanelle L, Sentjurc M, Grimalt JO, Cimerman GN, Plemenitas A (2004) Salt-induced changes in lipid composition and membrane fluidity of halophilic yeast-like melanized fungi. Extremophiles 8:53–61.  https://doi.org/10.1007/s00792-003-0360-5 CrossRefPubMedGoogle Scholar
  30. 30.
    Van MG (2005) Cellular lipidomics. EMBO J 24(18):3159.  https://doi.org/10.1038/sj.emboj.7600798 CrossRefGoogle Scholar
  31. 31.
    Verma M, Sk Brar, Tyagi RD et al (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20.  https://doi.org/10.1016/j.bej.2007.05.012 CrossRefGoogle Scholar
  32. 32.
    Welti R, Li W, Li M et al (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002.  https://doi.org/10.1074/jbc.M205375200 CrossRefPubMedGoogle Scholar
  33. 33.
    Wenk MR (2010) Lipidomics: new tools and applications. Cell 143:888–895.  https://doi.org/10.1016/j.cell.2010.11.033 CrossRefPubMedGoogle Scholar
  34. 34.
    Xia J, Jones AD, Lau MW et al (2011) Comparative lipidomic profiling of xylose-metabolizing S. cerevisiae and its parental strain in different media reveals correlations between membrane lipids and fermentation capacity. Biotechnol Bioeng 108:12–21.  https://doi.org/10.1002/bit.22910 CrossRefPubMedGoogle Scholar
  35. 35.
    Xu P, Shen T, Liu WP et al (2013) The elicitation effect of pathogenic fungi on trichodermin production by Trichoderma brevicompactum. Sci World J.  https://doi.org/10.1155/2013/607102 Google Scholar
  36. 36.
    Xu P, Shen T, Zhan XH et al (2014) Antifungal activity of metabolites of the endophytic fungus Trichoderma brevicompactum from garlic. Braz J Microbiol 45(1):248.  https://doi.org/10.1590/s1517-83822014005000036 CrossRefGoogle Scholar
  37. 37.
    Yan X, Chen D, Xu J et al (2011) Profiles of photosynthetic glycerolipids in three strains of Skeletonema, determined by UPLC-Q-TOF-MS. J Appl Phycol 23(2):271–282.  https://doi.org/10.1007/s10811-010-9553-3 CrossRefGoogle Scholar
  38. 38.
    Yin GL, Wang WM, Sha S et al (2010) Inhibition and control effects of the ethyl acetate extract of Trichoderma harzianum fermented broth against Botrytis cinerea. Afr J Microbiol Res 4(15):1647–1653Google Scholar

Copyright information

© Society for Industrial Microbiology and Biotechnology 2019

Authors and Affiliations

  1. 1.School of Life Science and TechnologyHarbin Institute of TechnologyHarbin CityChina
  2. 2.School of PharmacyQiqihar Medical UniversityQiqihar CityChina

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