Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails
Abstract Background Global warming is redrawing the map for invasive species, spotlighting the globally harmful giant African snail as a major ecological disruptor and public health threat. Known for harboring extensive antibiotic resistance genes (ARGs) and human pathogens, it remains uncertain whe...
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| Format: | Article |
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BMC
2025-02-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-025-02044-7 |
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| author | Yiyue Zhang Hong-Zhe Li Martin Breed Zhonghui Tang Li Cui Yong-Guan Zhu Xin Sun |
| author_facet | Yiyue Zhang Hong-Zhe Li Martin Breed Zhonghui Tang Li Cui Yong-Guan Zhu Xin Sun |
| author_sort | Yiyue Zhang |
| collection | DOAJ |
| description | Abstract Background Global warming is redrawing the map for invasive species, spotlighting the globally harmful giant African snail as a major ecological disruptor and public health threat. Known for harboring extensive antibiotic resistance genes (ARGs) and human pathogens, it remains uncertain whether global warming exacerbates these associated health risks. Methods We use phenotype-based single-cell Raman with D2O labeling (Raman-D2O) and genotype-based metagenomic sequencing to investigate whether soil warming increases active antibiotic-resistant bacteria (ARBs) in the gut microbiome of giant African snails. Results We show a significant increase in beta-lactam phenotypic resistance of active ARBs with rising soil temperatures, mirrored by a surge in beta-lactamase genes such as SHV, TEM, OCH, OKP, and LEN subtypes. Through a correlation analysis between the abundance of phenotypically active ARBs and genotypically ARG-carrying gut microbes, we identify species that contribute to the increased activity of antibiotic resistome under soil warming. Among 299 high-quality ARG-carrying metagenome-assembled genomes (MAGs), we further revealed that the soil warming enhances the abundance of “supercarriers” including human pathogens with multiple ARGs and virulence factors. Furthermore, we identified elevated biosynthetic gene clusters (BGCs) within these ARG-carrying MAGs, with a third encoding at least one BGC. This suggests a link between active ARBs and secondary metabolism, enhancing the environmental adaptability and competitive advantage of these organisms in warmer environments. Conclusions The study underscores the complex interactions between soil warming and antibiotic resistance in the gut microbiome of the giant African snail, highlighting a potential escalation in environmental health risks due to global warming. These findings emphasize the urgent need for integrated environmental and health strategies to manage the rising threat of antibiotic resistance in the context of global climate change. Video Abstract |
| format | Article |
| id | doaj-art-a8cb3a47a9b5412e984b7dd3c6cb33c5 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj-art-a8cb3a47a9b5412e984b7dd3c6cb33c52025-02-09T12:46:43ZengBMCMicrobiome2049-26182025-02-0113111510.1186/s40168-025-02044-7Soil warming increases the active antibiotic resistome in the gut of invasive giant African snailsYiyue Zhang0Hong-Zhe Li1Martin Breed2Zhonghui Tang3Li Cui4Yong-Guan Zhu5Xin Sun6State Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of SciencesState Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of SciencesCollege of Science & Engineering, Flinders UniversityState Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of SciencesState Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of SciencesState Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of SciencesState Key Laboratory for Ecological Security of Regions and Cities, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of SciencesAbstract Background Global warming is redrawing the map for invasive species, spotlighting the globally harmful giant African snail as a major ecological disruptor and public health threat. Known for harboring extensive antibiotic resistance genes (ARGs) and human pathogens, it remains uncertain whether global warming exacerbates these associated health risks. Methods We use phenotype-based single-cell Raman with D2O labeling (Raman-D2O) and genotype-based metagenomic sequencing to investigate whether soil warming increases active antibiotic-resistant bacteria (ARBs) in the gut microbiome of giant African snails. Results We show a significant increase in beta-lactam phenotypic resistance of active ARBs with rising soil temperatures, mirrored by a surge in beta-lactamase genes such as SHV, TEM, OCH, OKP, and LEN subtypes. Through a correlation analysis between the abundance of phenotypically active ARBs and genotypically ARG-carrying gut microbes, we identify species that contribute to the increased activity of antibiotic resistome under soil warming. Among 299 high-quality ARG-carrying metagenome-assembled genomes (MAGs), we further revealed that the soil warming enhances the abundance of “supercarriers” including human pathogens with multiple ARGs and virulence factors. Furthermore, we identified elevated biosynthetic gene clusters (BGCs) within these ARG-carrying MAGs, with a third encoding at least one BGC. This suggests a link between active ARBs and secondary metabolism, enhancing the environmental adaptability and competitive advantage of these organisms in warmer environments. Conclusions The study underscores the complex interactions between soil warming and antibiotic resistance in the gut microbiome of the giant African snail, highlighting a potential escalation in environmental health risks due to global warming. These findings emphasize the urgent need for integrated environmental and health strategies to manage the rising threat of antibiotic resistance in the context of global climate change. Video Abstracthttps://doi.org/10.1186/s40168-025-02044-7Active antibiotic resistomeAntimicrobial resistanceSoil warmingSingle-cell Raman spectroscopyHuman bacterial pathogen |
| spellingShingle | Yiyue Zhang Hong-Zhe Li Martin Breed Zhonghui Tang Li Cui Yong-Guan Zhu Xin Sun Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails Microbiome Active antibiotic resistome Antimicrobial resistance Soil warming Single-cell Raman spectroscopy Human bacterial pathogen |
| title | Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails |
| title_full | Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails |
| title_fullStr | Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails |
| title_full_unstemmed | Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails |
| title_short | Soil warming increases the active antibiotic resistome in the gut of invasive giant African snails |
| title_sort | soil warming increases the active antibiotic resistome in the gut of invasive giant african snails |
| topic | Active antibiotic resistome Antimicrobial resistance Soil warming Single-cell Raman spectroscopy Human bacterial pathogen |
| url | https://doi.org/10.1186/s40168-025-02044-7 |
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