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Research Article | Open Access

Genome sequence and metabolic analysis of Pseudomonas fragi unveil the meat spoilage and CO2-antibacterial mechanism under high-oxygen modified atmosphere packaging

Jun Yang1,2, Yikun Xu1, Yimin Zhang1,2, Rongrong Liang1,2, Lixian Zhu1,2, Yanwei Mao1,2, Xin Luo1,2, Xiaoyin Yang1,2 ()
Laboratory of Meat Processing and Quality Control, College of Food Science and Engineering, Shandong Agricultural University,Tai’an 271018, China
National R&D Center for Beef Processing Technology, Tai’an 271018, China
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Abstract

Pseudomonas fragi is a predominant meat-borne spoilage bacterium that is sensitive to CO2 under high-oxygen modified atmosphere packaging (HiOx-MAP). This study was designed to reveal the spoilage potential of a popular wild-type P. fragi T1 in HiOx-MAP beef by whole genome sequencing, and explore the bacterial metabolic response to CO2 utilizing combined metabolomic and volatile organic compounds (VOCs) analysis, under treatment (CO2-enriched) HiOx-MAP (TMAP, 50% O2/40% CO2/10% N2) or control (non-CO2) HiOx-MAP (CMAP, 50% O2/50% N2) during chilled storage. Results showed that the strain P. fragi T1 was endued with spoilage-related genes associated with protease, lipase and esterase production, amino acid metabolism, carbon metabolism, sulfur metabolism, and putrescine metabolism, which was responsible for the hydrolysis of meat protein and lipid, as well as off-odor formation. The growth of P. fragi under CMAP resulted in the production of VOCs, such as diacetyl, 1-undecene, 2-undecanone, nonanal, (Z)-5-decen-1-ol, and (E)-2-octenal, etc. The TMAP declined above VOCs concentrations significantly (P < 0.05) by inhibiting P. fragi growth and regulating its metabolic activities. The metabolomic analysis further manifested that CO2 inhibited the P. fragi growth by decreasing cell membrane fluidity, disturbing energy metabolism, and inhibiting amino acid metabolism and nucleotide biosynthesis. This work provides valuable information for understanding the P. fragi-induced meat spoilage phenomena, and the antibacterial mechanism of CO2 against P. fragi.

Keywords

Pseudomonas fragiCO2 antibacterial mechanismmetabolomicswhole genome sequencevolatile organic compounds

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Food Science of Animal Products
Volume 2 Issue 4,
December 2024
Article number: 9240084
DOI: 10.26599/FSAP.2024.9240084
Cite this article:
Yang J, Xu Y, Zhang Y, et al. Genome sequence and metabolic analysis of Pseudomonas fragi unveil the meat spoilage and CO2-antibacterial mechanism under high-oxygen modified atmosphere packaging. Food Science of Animal Products, 2024, 2(4): 9240084. https://doi.org/10.26599/FSAP.2024.9240084
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Gene prediction and annotation summary of P. fragi T1.

ItemResult
Gene number4 757
Gene total length (bp)4 627 302
Gene average length (bp)972
GC content (%)58.08
Maximum length (bp)10 251
Minimum length (bp)90
tRNA number79
5S rRNA number9
16S rRNA number8
23S rRNA number8

Spoilage-related pathways and genes of P. fragi T1 by KEGG analysis.

FunctionKOKO functionEnzyme
Note: - Indicates the EC number is lacking.
Proteolysis processK07263Zinc proteaseEC:3.4.24.-
K04774Serine protease SohBEC:3.4.21.-
K04691Serine protease DegSEC:3.4.21.-
Glycerophospholipid metabolism/glycerolipid metabolismK01126Glycerophosphoryl diester phosphodiesteraseEC:3.1.4.46
K01046Triacylglycerol lipaseEC:3.1.1.3
Biosynthesis of amino acidsK00620Glutamate N-acetyltransferase/amino-acid N-acetyltransferaseEC:2.3.1.35/2.3.1.1
K01620Threonine aldolaseEC:4.1.2.48
K01752L-serine dehydrataseEC:4.3.1.17
K01478Arginine deiminaseEC:3.5.3.6
K01585Arginine decarboxylaseEC:4.1.1.19
K01438Acetylornithine deacetylaseEC:3.5.1.16
K00930Acetylglutamate kinaseEC:2.7.2.8
K01581Ornithine decarboxylaseEC:4.1.1.17
K00928Aspartate kinaseEC:2.7.2.4
K00789S-Adenosylmethionine synthetaseEC:2.5.1.6
K00926Carbamate kinaseEC:2.7.2.2
K01652Acetolactate synthase I/II/III large subunitEC:2.2.1.6
K01653Acetolactate synthase I/III small subunitEC:2.2.1.6
K00812Aspartate aminotransferaseEC:2.6.1.1
K00611Ornithine carbamoyltransferaseEC:2.1.3.3
K00640Serine O-acetyltransferaseEC:2.3.1.30
K14682Amino-acid N-acetyltransferaseEC:2.3.1.1
K000523-Isopropylmalate dehydrogenaseEC:1.1.1.85
K00145N-Acetyl-γ-glutamyl-phosphate reductaseEC:1.2.1.38
Sulfur metabolismK01011Thiosulfate/3-mercaptopyruvate sulfurtransferaseEC:2.8.1.1/2.8.1.2
K02439Thiosulfate sulfurtransferaseEC:2.8.1.1
K15553Sulfonate transport system substrate-binding protein-
K15554Sulfonate transport system permease protein-
K15555Sulfonate transport system ATP-binding proteinEC:3.6.3.-
K17218Sulfide:quinone oxidoreductaseEC:1.8.5.4
K02048Sulfate/thiosulfate transport system substrate-binding protein-
K02046Sulfate/thiosulfate transport system permease protein-
K02045Sulfate/thiosulfate transport system ATP-binding proteinEC:7.3.2.3
K00957Sulfate adenylyltransferase subunit 2EC:2.7.7.4
K00390Phosphoadenosine phosphosulfate reductaseEC:1.8.4.8 (1.8.4.10)
K10764O-Succinylhomoserine sulfhydrylaseEC:2.5.1.-
K01738Cysteine synthaseEC:2.5.1.47
Carbon metabolismK18118Succinyl-CoA:acetate CoA-transferaseEC:2.8.3.18
K01903Succinyl-CoA synthetase beta subunitEC:6.2.1.5
K01902Succinyl-CoA synthetase alpha subunitEC:6.2.1.5
K00640Serine O-acetyltransferaseEC:2.3.1.30
K00948Ribose-phosphate pyrophosphokinaseEC:2.7.6.1
K00873Pyruvate kinaseEC:2.7.1.40
K00627Pyruvate dehydrogenase E2 component (dihydrolipoamide acetyltransferase)EC:2.3.1.12
K00163Pyruvate dehydrogenase E1 componentEC:1.2.4.1
K01960Pyruvate carboxylase subunit BEC:6.4.1.1
K01959Pyruvate carboxylase subunit AEC:6.4.1.1
K01690Phosphogluconate dehydrataseEC:4.2.1.12
K01595Phosphoenolpyruvate carboxylaseEC:4.1.1.31
K13788Phosphate acetyltransferaseEC:2.3.1.8
K01638Malate synthaseEC:2.3.3.9
K01637Isocitrate lyaseEC:4.1.3.1
K00031Isocitrate dehydrogenaseEC:1.1.1.42
Carbon metabolismK00600Glycine hydroxymethyltransferaseEC:2.1.2.1
K00281Glycine dehydrogenaseEC:1.4.4.2
K00018Glycerate dehydrogenaseEC:1.1.1.29
K00134Glyceraldehyde 3-phosphate dehydrogenaseEC:1.2.1.12
K00036Glucose-6-phosphate 1-dehydrogenaseEC:1.1.1.49 (1.1.1.363)
K00851GluconokinaseEC:2.7.1.12
K00845GlucokinaseEC:2.7.1.2
K01679Fumarate hydratase, class IIEC:4.2.1.2
K01676Fumarate hydratase, class IEC:4.2.1.2
K00382Dihydrolipoamide dehydrogenaseEC:1.8.1.4
K01647Citrate synthaseEC:2.3.3.1
K03781CatalaseEC:1.11.1.6
K00605AminomethyltransferaseEC:2.1.2.10
K00249Acyl-coenzyme A dehydrogenaseEC:1.3.8.7
K01681Aconitate hydrataseEC:4.2.1.3
K010576-PhosphogluconolactonaseEC:3.1.1.31
K000336-Phosphogluconate dehydrogenaseEC:1.1.1.44 (1.1.1.343)
K006582-Oxoglutarate dehydrogenase E2 component (dihydrolipoamide succinyltransferase)EC:2.3.1.61
K001642-Oxoglutarate dehydrogenase E1 componentEC:1.2.4.2
K008742-Dehydro-3-deoxygluconokinaseEC:2.7.1.45

Changes in volatile compounds (μg/L) of beef juice stored under both MAP systems during chilled storage.

CompoundsPackagingInoculation typeStorage time (day)Standard errorP value
014812
Note: Different superscript lowercase letters indicate significant differences between storage times (P < 0.05). TMAP: 50% O2/40% CO2/10% N2; CMAP: 50% O2/50% N2.
DiacetylTMAPP. fragi0.32< 0.001
Saline
CMAPP. fragi4.41
Saline
(Z)-5-Decen-1-olTMAPP. fragi0.410.010
Saline
CMAPP. fragi1.57b3.44a
Saline
1-UndeceneTMAPP. fragi1.37< 0.001
Saline
CMAPP. fragi28.52b39.59a
Saline
2-UndecanoneTMAPP. fragi0.20a0.30a0.15a0.670.029
Saline
CMAPP. fragi0.11b0.18b1.68b5.33a
Saline
(E)-2-OctenalTMAPP. fragi0.100.048
Saline
CMAPP. fragi0.68
Saline