Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (11): 2172-2185.doi: 10.3864/j.issn.0578-1752.2023.11.011

• FOOD SCIENCE AND ENGINEERING • Previous Articles     Next Articles

Effects of nuoB on the Biofilm Formation and Cellular Metabolism of Meat-Borne Pseudomonas fragi During Chilled Storage

WU YaJie1(), TAN Song1, CHEN YuPing1, NIU AJuan1, LIU YuXin1, WANG GuangYu1(), XU XingLian2, QIU WeiFen1   

  1. 1 College of Food Science and Engineering/Collaborative Innovation Center for Modern Grain Circulation and Safety, Nanjing University of Finance and Economics, Nanjing 210023
    2 College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095
  • Received:2022-10-25 Accepted:2022-12-21 Online:2023-06-01 Published:2023-06-19

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Abstract:

【Objective】This paper focused on the impacts of nuoB on the biofilm formation and cell metabolism in Pseudomonas fragi (P. fragi), so as to further reveal the regulatory mechanism of nuoB in the spoilage of chilled meat contaminated with P. fragi, and to provide a theoretical basis for developing effective preservation system of chilled meat. 【Method】P. fragi NMC25 and its nuoB-mutant strain were used in the present study, and the differences in the spatial structure of biofilms were observed by confocal laser scanning microscopy (CLSM). The changes in biofilm composition were tested by the cell enumeration and the analysis of the extracellular polymeric substances. In addition, the ultra-high performance liquid chromatography coupled with mass spectrometry (UHPLC-MS/MS) was employed to investigate the alterations of nuoB-related metabolite abundance. 【Result】CLSM images showed that cells in the biofilms of wild-type strains cultivated in situ was highly dense, nematic ordering, whereas ΔnuoB displayed relatively disorganized and sparse arrangement. Additionally, cell enumeration revealed insignificant differences between the wild-type and mutant biofilms regardless of the difference of culture medium. The result indicated that the mutants did not change significantly in their ability to grow as biofilm on the surface of TSA or meat sample. For extracellular polymeric substances from biofilms in situ, the protein and carbohydrate contents of ΔnuoB were significantly higher (P<0.01, P<0.05, respectively) than those of wild-type strains, indicating that nuoB affected the secretion of extracellular polymers by P. fragi. The metabolomics results revealed a clear separation between the wild and mutant groups in an orthogonal partial least squares discriminant analysis model (R2X=0.481, R2Y=0.977, Q2=0.909), which suggested that the metabolites of the mutants had changed markedly. In the model, differentially expressed metabolites were screened, including 2-hydroxycinnamic acid, L-tyrosine, L-phenylalanine, DL-tryptophan, 17(S)-HETE, and 5-OxoETE. Pathway mapping analysis was conducted based on the chosen candidates. In total, the major metabolic pathways included fatty acid biosynthesis, unsaturated fatty acid biosynthesis, riboflavin metabolism, 2-oxocarboxylic acid metabolism, purine metabolism, cyanogenic amino acid metabolism, and phenylalanine metabolism. 【Conclusion】The disruption of nuoB stimulated significant variations in the spatial structure of the P. fragi biofilm grown in situ, promoting the biosynthesis of extracellular polymeric substances and affecting intracellular metabolic pathways, such as carbon, nucleotide, lipid, and amino acid metabolism.

Key words: Pseudomonas fragi, nuoB, biofilm, extracellular polymeric substances, cell metabolism

Table 1

The gradient elution of mobile phase"

时间 Time (min) A (%) B (%)
0 98 2
1.5 98 2
12 0 100
14 0 100
14.1 98 2
17.0 98 2

Fig. 1

Images of macrocolony biofilm formation of the P. fragi NMC25 and ΔnuoB Control: Biofilms cultivated on TSA without transfer; A: P. fragi NMC25 biofilms; B: ΔnuoB biofilms"

Fig. 2

Confocal laser scanning microscopy images of P. fragi NMC25 and ΔnuoB biofilms Green cells represent live cells and red cells represent dead cells. A, B indicate the spatial structure in NMC25 and ΔnuoB biofilms in situ, respectively; C, D indicate the spatial structure in NMC25 and ΔnuoB biofilms cultivated on TSA, respectively"

Table 2

Cell counts, and EPS content in the biofilms of two strains of P. fragi grown on different culture mediums"

细菌数量 Bacterial counts
(log CFU/colony)		 蛋白质 Protein
(µg/mg-wet-cell-biomass)		 总糖 Carbohydrate
(µg/mg-wet-cell-biomass)		 蛋白/总糖
Protein/Carbohydrate ratio
原位培养 In situ cultivation
NMC25 9.92±0.07 38.61±1.92 14.16±0.69 2.73±0.23
ΔnuoB 9.86±0.06 46.65±1.62** 16.55±0.93* 2.82±0.08
TSA培养 TSA cultivation
NMC25 10.11±0.09 0.61±0.36 17.23±0.80 0.04±0.02
ΔnuoB 10.05±0.03 2.10±0.63** 17.40±0.77 0.12±0.04**

Fig. 3

OPLS-DA score plot (A), loading plot (B), and permutation plot (C) of metabolite variation between the NMC25 and ΔnuoB groups"

Fig. 4

Volcano plot (A) and VIP scores (B) of top 15 important featured metabolites between NMC25 and ΔnuoB strains"

Fig. 5

The bubble charts of top 20 metabolic pathways between the NMC25 and ΔnuoB groups"

Fig. 6

Proposed schematic of intracellular metabolic alterations affected by nuoB Metabolites marked in green or red represent significantly higher or lower concentrations in the ΔnuoB group as compared to the NMC25 group, respectively (VIP>1, P<0.05). Upward and downward arrows beside metabolites indicate increased and decreased changes in addition to discriminant metabolites, respectively (|lg2FC|>0.58 or VIP>1). Metabolites colored in black without arrow represents similar level between the NMC25 group and ΔnuoB group, while metabolites in italic were not detected"

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