Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure

Tetracycline antibiotics play a vital role in animal husbandry, primarily employed to uphold the health of livestock and poultry. Consequently, when manure is reintegrated into farmland, tetracycline antibiotics can persist in the soil. Simultaneously, to ensure optimal crop production, organochlori...

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Main Authors: Haoliang Wang, Wei Wang, Fenhua Jin, Jeremy N. Marchant-Forde, Jiandui Mi, Lipeng Ding, Xindi Liao, Yinbao Wu, Yan Wang
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651323014227
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author Haoliang Wang
Wei Wang
Fenhua Jin
Jeremy N. Marchant-Forde
Jiandui Mi
Lipeng Ding
Xindi Liao
Yinbao Wu
Yan Wang
author_facet Haoliang Wang
Wei Wang
Fenhua Jin
Jeremy N. Marchant-Forde
Jiandui Mi
Lipeng Ding
Xindi Liao
Yinbao Wu
Yan Wang
author_sort Haoliang Wang
collection DOAJ
description Tetracycline antibiotics play a vital role in animal husbandry, primarily employed to uphold the health of livestock and poultry. Consequently, when manure is reintegrated into farmland, tetracycline antibiotics can persist in the soil. Simultaneously, to ensure optimal crop production, organochlorine pesticides (OCPs) are frequently applied to farmland. The coexistence of tetracycline antibiotics and OCPs in soil may lead to an increased risk of transmission of tetracycline resistance genes (TRGs). Nevertheless, the precise mechanism underlying the effects of OCPs on tetracycline antibiotics and TRGs remains elusive. In this study, we aimed to investigate the effects of OCPs on soil tetracycline antibiotics and TRGs using different concentrations of doxycycline (DOX) and pentachlorophenol (PCP). The findings indicate that PCP and DOX mutually impede their degradation in soil. Furthermore, our investigation identifies Sphingomonas and Bacillus as potential pivotal microorganisms influencing the reciprocal inhibition of PCP and DOX. Additionally, it is observed that the concurrent presence of PCP and DOX could impede each other's degradation by elevating soil conductivity. Furthermore, we observed that a high concentration of PCP (10.7 mg/kg) reduced the content of efflux pump tetA, ribosome protective protein tetM, tetQ, and passivating enzyme tetX. In contrast, a low PCP concentration (6.4 mg/kg) only reduced the content of ribosome protective protein tetQ. This suggests that PCP may reduce the relative abundance of TRGs by altering the soil microbial community structure and inhibiting the potential host bacteria of TRGs. These findings have significant implications in understanding the combined pollution of veterinary antibiotics and OCPs. By shedding light on the interactions between these compounds and their impact on microbial communities, this study provides a theoretical basis for developing strategies to manage and mitigate their environmental impact, and may give some information regarding the sustainable use of antibiotics and pesticides to ensure the long-term health and productivity of agricultural systems.
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spelling doaj.art-bdb1d73f9fb445c1a6ad76787a6b91f52024-02-03T06:34:22ZengElsevierEcotoxicology and Environmental Safety0147-65132024-02-01271115918Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structureHaoliang Wang0Wei Wang1Fenhua Jin2Jeremy N. Marchant-Forde3Jiandui Mi4Lipeng Ding5Xindi Liao6Yinbao Wu7Yan Wang8Heyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, ChinaHeyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, ChinaHeyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, ChinaLivestock Behavior Research Unit, USDA-ARS, West Lafayette, 47906 IN, USA; Corresponding author.Heyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, China; Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China; National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, ChinaHeyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, China; Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China; National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, China; Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China; National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, China; Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, South China Agricultural University, Guangzhou 510642, China; National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, China; Corresponding author at: Heyuan Branch, Guangdong Provincial Laboratory of Lingnan Modern Agricultural Science and Technology, College of Animal Science, South China Agricultural University, Guangzhou, China.Tetracycline antibiotics play a vital role in animal husbandry, primarily employed to uphold the health of livestock and poultry. Consequently, when manure is reintegrated into farmland, tetracycline antibiotics can persist in the soil. Simultaneously, to ensure optimal crop production, organochlorine pesticides (OCPs) are frequently applied to farmland. The coexistence of tetracycline antibiotics and OCPs in soil may lead to an increased risk of transmission of tetracycline resistance genes (TRGs). Nevertheless, the precise mechanism underlying the effects of OCPs on tetracycline antibiotics and TRGs remains elusive. In this study, we aimed to investigate the effects of OCPs on soil tetracycline antibiotics and TRGs using different concentrations of doxycycline (DOX) and pentachlorophenol (PCP). The findings indicate that PCP and DOX mutually impede their degradation in soil. Furthermore, our investigation identifies Sphingomonas and Bacillus as potential pivotal microorganisms influencing the reciprocal inhibition of PCP and DOX. Additionally, it is observed that the concurrent presence of PCP and DOX could impede each other's degradation by elevating soil conductivity. Furthermore, we observed that a high concentration of PCP (10.7 mg/kg) reduced the content of efflux pump tetA, ribosome protective protein tetM, tetQ, and passivating enzyme tetX. In contrast, a low PCP concentration (6.4 mg/kg) only reduced the content of ribosome protective protein tetQ. This suggests that PCP may reduce the relative abundance of TRGs by altering the soil microbial community structure and inhibiting the potential host bacteria of TRGs. These findings have significant implications in understanding the combined pollution of veterinary antibiotics and OCPs. By shedding light on the interactions between these compounds and their impact on microbial communities, this study provides a theoretical basis for developing strategies to manage and mitigate their environmental impact, and may give some information regarding the sustainable use of antibiotics and pesticides to ensure the long-term health and productivity of agricultural systems.http://www.sciencedirect.com/science/article/pii/S0147651323014227Organochlorine pesticidesTetracycline resistance genesCoexistenceMicroorganismsDegradation
spellingShingle Haoliang Wang
Wei Wang
Fenhua Jin
Jeremy N. Marchant-Forde
Jiandui Mi
Lipeng Ding
Xindi Liao
Yinbao Wu
Yan Wang
Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
Ecotoxicology and Environmental Safety
Organochlorine pesticides
Tetracycline resistance genes
Coexistence
Microorganisms
Degradation
title Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
title_full Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
title_fullStr Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
title_full_unstemmed Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
title_short Pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
title_sort pentachlorophenol affects doxycycline and tetracycline resistance genes in soil by altering microbial structure
topic Organochlorine pesticides
Tetracycline resistance genes
Coexistence
Microorganisms
Degradation
url http://www.sciencedirect.com/science/article/pii/S0147651323014227
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