Antimicrobial resistance (AMR) is one of the top ten threats to global public health that causes significant damage to global health (human, animal, plant, and environmental health) and the economy.Salmonella entericais a major cause of global foodborne and invasive diseases, and AMRSalmonellaisolates pose a serious threat to public healthand have been listed in the 2024 World Health Organization bacterial priority pathogens list.

1、The ecological distribution and transfer of antibiotic resistance genes (ARGs) in animal, human, and environmental microbiome

First, the diversity and ecological distribution of ARGs in the LPMs in China were revealed using the metagenomic method on a large scale, for the first time, indicating that the LPMs were a huge reservoir of ARGs. Second, more diversified ARGs were identified in the LPM samples than in chicken farms, and more abundant ARGs were found in the LPM workers than in those who have no contact with LPMs, suggesting that the live poultry trade contributes to the spread of AMR within the One Health strategy. Third, we used both metagenomic and metatranscriptomic approaches to comprehensively reveal the abundance, diversity, and expression of ARGs in human, chicken, and pig gut microbiomes in China. Metatranscriptomic analysis revealed that 49.4, 66.5, and 56.6% of ARGs identified in human, chicken, and pig gut microbiota, respectively, were expressed, indicating that a large proportion of ARGs were not transcriptionally active. We also constructed a chicken multi-kingdom microbiome catalog (CMKMC), including 18,201 bacterial, 225 archaeal, and 33,411 viral genomes, and annotated over 6,076,006 protein-coding genes by integrating 135 chicken gut metagenomes and publicly available metagenome-assembled genomes from ten countries. A total of 812 and 240 MAGs in our dataset were putative novel species and genera, respectively, far beyond what was previously reported. Moreover, a large number of acquired ARGs were identified in the gut microbiome of migratory birds, and the landscapes of bacterial microbial and ARGs of 10 migratory bird species were drawn, suggesting that the migration of wild birds may be one of the important ways for the global spread of ARGs and AR pathogens.

2、The temporal dynamics of antimicrobial-resistant Salmonella enterica and predominant serovars in China

Here, taking the One Health strategy, we used >35,000 Salmonella enterica isolates to explore the temporal and spatial dynamics of dominant serovars in China. We found that Salmonella Typhimurium was the dominant serovar causing human infection in China, which was consistent with Australia but inconsistent with North American and European countries. The proportion of Salmonella serovars Typhimurium, London, Rissen, Corvallis, Meleagridis, Kentucky, and Goldcoast showed an increasing trend in recent years. The number of ARGs per isolate increased by 1.84 and 2.69 times of human and non-human origins, respectively, spanning recent 14 years. The proportion of AMR Salmonella isolates had an increasing trend in recent years, especially beta-lactam, quinolone, tetracycline, and rifampicin resistance. A total of 200 STs were identified, higher diversity of STs in S. Typhimurium than in other serovars, and ST34 from pig and ST19 from chicken origin, were mainly associated with isolates causing child and adult gastro-infection, respectively. Moreover, we describe the first global report of the identification of plasmid-mediated tigecycline resistance gene tet(X4) in a multi-drug resistance S. enterica serovar Llandoff strain ST8300 isolated from a man’s fecal sample in China. Our results fill in the data gap on the trends of dominant serovars and antimicrobial resistance of Salmonella enterica in China. These data provide useful information for public health decision-makers prioritizing interventions for foodborne diseases and food safety.

3、Construction and application of the Chinese Local Salmonella Genome Database Version 2 (CLSGDB v2)

After understanding the spatial and temporal distribution characteristics of the dominant serovars of Salmonella, we use 1,962 Salmonella isolates collected from 22 Chinese provinces and add 6,035 publicly available genomes to build the Chinese local Salmonella genome database version 2 (CLSGDB v2) represent ing 30 Chinese provinces, covering 1905–2022. Using the CLSGDB v2, we mapped the landscape and spatiotemporal dynamics of antimicrobial resistance markers, virulome, and mobilome in Salmonella. Interestingly, economic, climatic, and social factors can drive the rise of AMR in Salmonella was observed. Finally, we release the CLSGDB v2 as an open-access database and thus can assist surveillance studies tracking 164 Salmonella enterica serovars and 295 sequence types across the globe. The CLSGDB v2 is freely available at https://nmdc.cn/clsgdbv2. The CLSGDBv2 has been accessed and downloaded nearly 120,000 times by 35 countries and regions on 6 continents (as of October 31, 2024).

4、Representative papers

1. Wang Y^#, Liu Y^#, Lyu N, Li Z, Ma S, Cao D, Pan Y, Hu Y, Huang H, Gao GF*, Xu X*, on behalf of the Bacterium-learning Union; Zhu B*. The temporal and spatial dynamics of antimicrobial-resistant Salmonella enterica and predominant serovars in China. Natl Sci Rev. 2023; 10(3): nwac269. (ESI Highly cited papers)

2. Wang Y^#, Xu X^#, Zhu B, Lyu N, Liu Y, Ma S, Jia S, Wan B, Du Y, Zhang G*, Gao GF*. Genomic analysis of almost 8,000 Salmonella genomes reveals drivers and landscape of antimicrobial resistance in China. Microbiol Spectr. 2023; 11(6): e0208023.

3. Wang Y, Lyu N, Liu F, Liu J, Bi Y, Zhang Z, Ma S, Cao J, Song X, Wang A, Zhang G, Hu Y*, Zhu B*, Gao GF*. More diversified antibiotic resistance genes in chickens and workers of the live poultry markets. Environ Int. 2021; 153: 106534.

4. Wang Y^#, Hu Y^#, Liu F, Cao J, Lv N, Zhu B, Zhang G, Gao GF*. Integrated metagenomic and metatranscriptomic profiling reveals differentially expressed resistomes in human, chicken, and pig gut microbiomes. Environ Int. 2020; 138: 105649.

5. Wang Y^#, Hu Y^#, Cao J, Bi Y, Lv N, Liu F, Liang S, Shi Y, Jiao X*, Gao GF*, Zhu B*. Antibiotic resistance gene reservoir in live poultry markets. J Infection. 2019; 78(6): 445-453. (Editor’s choice)

6. Cao J^#, Hu Y^#, Liu F^#, Wang Y, Bi Y, Lv N, Li J, Zhu B*, Gao GF*. Metagenomic analysis reveals the microbiome and resistome in migratory birds. Microbiome. 2020, 8, 26.

7. Shen Y^#, Zhang R^#, Shao D, Yang L, Lu J, Liu C, Wang X, Jiang J, Wang B, Wu C, Parkhill J, Wang Y, Walsh TR*, Gao GF*, Shen Z*. Genomic shift in population dynamics of mcr-1-positive Escherichia coli in human carriage. Genom Proteom Bioinf. 2022, 20(6): 1168-1179.

8. Yin W^#, Ling Z^#, Dong Y^#, Qiao L^#, Shen Y^#, Liu Z, Wu Y, Li W, Zhang R, Walsh TR, Dai C, Li J, Yang H, Liu D, Wang Y*, Gao GF*, Shen J*. Mobile colistin resistance enzyme MCR-3 facilitates bacterial evasion of host phagocytosis. Adv Sci, 2021, 8(18): e2101336.