Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism

ABSTRACT Nettle showed several benefits for animals as an unconventional feed source, but it is difficult to ensile in order to be better utilized. Recently, nettle has been utilized to alternate alfalfa as ruminant feed, but it is usually poor in ensiling quality. To determine the endogenous compon...

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Main Authors: Rongzheng Huang, Yuxin Chai, Shuangming Li, Yongcheng Chen, Shu'an Jia, Chunhui Ma, Fanfan Zhang
Format: Article
Language:English
Published: American Society for Microbiology 2025-06-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.02667-24
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author Rongzheng Huang
Yuxin Chai
Shuangming Li
Yongcheng Chen
Shu'an Jia
Chunhui Ma
Fanfan Zhang
author_facet Rongzheng Huang
Yuxin Chai
Shuangming Li
Yongcheng Chen
Shu'an Jia
Chunhui Ma
Fanfan Zhang
author_sort Rongzheng Huang
collection DOAJ
description ABSTRACT Nettle showed several benefits for animals as an unconventional feed source, but it is difficult to ensile in order to be better utilized. Recently, nettle has been utilized to alternate alfalfa as ruminant feed, but it is usually poor in ensiling quality. To determine the endogenous component influencing ensiling, we investigated the effect of Pediococcus on the characteristics of nettle silage and the mechanism of action of these substances against Pediococcus. Inoculation with Pediococcus pentosaceus decreased the relative abundance of Clostridium sensu stricto 15 by 85.95% in the middle fermentation stage of nettle silage (30 d), with a 24.74% decrease in the ammonia content (P<0.05). In the correlation analysis, 4-pentenoic acid showed an extremely significant negative correlation with Pediococcus spp. in nettle silage (P < 0.001). After 4-pentenoic acid treatment, the most downregulated proteins were involved in the ribosome pathway (30 differentially expressed proteins), and then in the glycolysis/gluconeogenesis, pyruvate metabolism, and fatty acid synthesis pathways (particularly for accA, accD, and fabG). The mechanism of action of 4-pentenoic acid against P. pentosaceus mainly involves inhibition of fatty acid synthesis and decreased the expression of acid tolerance proteins. The present study will give new insights into silage fermentation and provide new clues for better ensiling of nettle.IMPORTANCENettle has attracted the attention of scientists due to its several benefits for animals as non-conventional feed sources. However, as for challenge, nettle is difficult to ensile (poor quality), which is an obstacle for nettle use. In the present manuscript, we investigated the effect of Pediococcus on the characteristics of nettle silage and clarified the mechanisms of 4-pentenoic acid against Pediococcus. Our findings suggested that P. pentosaceus could improve nettle silage quality at a significant level through decreased production of ammonia (decline percentage was 21.41%–31.73%) during ensiling, while it could not well improve the quality of nettle silage due to the interference effect of 4-pentenoic acid as an antibacterial substance. The mechanism of 4-pentenoic acid against P. pentosaceus was mainly through inhibition of fatty acid synthesis (fabG) and expression of acid tolerance protein (accA), resulting in destruction of the cell wall in P. pentosaceus. Our finding could give a new clue for better use of nettle silage.
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publisher American Society for Microbiology
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spelling doaj-art-b02eca92cf0d4f69a4ff14bff21b56b32025-08-20T03:07:23ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-06-0113610.1128/spectrum.02667-24Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanismRongzheng Huang0Yuxin Chai1Shuangming Li2Yongcheng Chen3Shu'an Jia4Chunhui Ma5Fanfan Zhang6Grassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaGrassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaGrassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaGrassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaGrassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaGrassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaGrassland Science, School of Animal Technology, Shihezi University, Shihezi, Xinjiang, ChinaABSTRACT Nettle showed several benefits for animals as an unconventional feed source, but it is difficult to ensile in order to be better utilized. Recently, nettle has been utilized to alternate alfalfa as ruminant feed, but it is usually poor in ensiling quality. To determine the endogenous component influencing ensiling, we investigated the effect of Pediococcus on the characteristics of nettle silage and the mechanism of action of these substances against Pediococcus. Inoculation with Pediococcus pentosaceus decreased the relative abundance of Clostridium sensu stricto 15 by 85.95% in the middle fermentation stage of nettle silage (30 d), with a 24.74% decrease in the ammonia content (P<0.05). In the correlation analysis, 4-pentenoic acid showed an extremely significant negative correlation with Pediococcus spp. in nettle silage (P < 0.001). After 4-pentenoic acid treatment, the most downregulated proteins were involved in the ribosome pathway (30 differentially expressed proteins), and then in the glycolysis/gluconeogenesis, pyruvate metabolism, and fatty acid synthesis pathways (particularly for accA, accD, and fabG). The mechanism of action of 4-pentenoic acid against P. pentosaceus mainly involves inhibition of fatty acid synthesis and decreased the expression of acid tolerance proteins. The present study will give new insights into silage fermentation and provide new clues for better ensiling of nettle.IMPORTANCENettle has attracted the attention of scientists due to its several benefits for animals as non-conventional feed sources. However, as for challenge, nettle is difficult to ensile (poor quality), which is an obstacle for nettle use. In the present manuscript, we investigated the effect of Pediococcus on the characteristics of nettle silage and clarified the mechanisms of 4-pentenoic acid against Pediococcus. Our findings suggested that P. pentosaceus could improve nettle silage quality at a significant level through decreased production of ammonia (decline percentage was 21.41%–31.73%) during ensiling, while it could not well improve the quality of nettle silage due to the interference effect of 4-pentenoic acid as an antibacterial substance. The mechanism of 4-pentenoic acid against P. pentosaceus was mainly through inhibition of fatty acid synthesis (fabG) and expression of acid tolerance protein (accA), resulting in destruction of the cell wall in P. pentosaceus. Our finding could give a new clue for better use of nettle silage.https://journals.asm.org/doi/10.1128/spectrum.02667-24Pediococcus pentosaceusnettle silage4-pentenoic acidammonia
spellingShingle Rongzheng Huang
Yuxin Chai
Shuangming Li
Yongcheng Chen
Shu'an Jia
Chunhui Ma
Fanfan Zhang
Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism
Microbiology Spectrum
Pediococcus pentosaceus
nettle silage
4-pentenoic acid
ammonia
title Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism
title_full Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism
title_fullStr Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism
title_full_unstemmed Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism
title_short Involvement of 4-pentenoic acid in causing quality deterioration of nettle silage: study of antibacterial mechanism
title_sort involvement of 4 pentenoic acid in causing quality deterioration of nettle silage study of antibacterial mechanism
topic Pediococcus pentosaceus
nettle silage
4-pentenoic acid
ammonia
url https://journals.asm.org/doi/10.1128/spectrum.02667-24
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