Ji Xing, Wang Yaxin, He Tao, Krüger-Haker Henrike, Wang Yang, Wu Congming, Schwarz Stefan, Sun Chengtao
National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of Ministry of Science and Technology, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, China.
mSystems. 2025 Sep 9:e0039725. doi: 10.1128/msystems.00397-25.
Livestock-associated methicillin-resistant (LA-MRSA) displays distinct geographical distribution patterns, with ST398 predominating in Europe and ST9 being the dominant lineage in Asia, particularly China. However, the mechanisms underlying these differences remain poorly understood. In this study, we evaluated the cell adhesion capacity, anti-phagocytic properties, and porcine nasal colonization potential of ST9 and ST398 strains isolated from China and Germany. Colonization dynamics and characteristics were further explored using 16S rRNA gene sequencing and metatranscriptomic analysis. Our findings revealed that LA-MRSA ST398 strains exhibited superior colonization capabilities, including enhanced cell adhesion, increased resistance to macrophage-mediated killing, and a stronger impact on nasal microbiota stability. Transcriptomic analyses during colonization indicated that ST398 strains prioritized pathways related to genome repair and amino acid metabolism, whereas ST9 strains, particularly those isolated from China, focused on carbohydrate metabolism. Although ST9 strains showed relatively weaker colonization capacity, the epidemic Chinese ST9 isolates carried multiple resistance genes [, (L), and (E)-(B)], exhibiting broad resistance to clinically important antibiotics including tylosin, florfenicol, and tetracyclines. This suggests that their prevalence in China may be maintained through antimicrobial selection pressure. With the implementation of stricter antibiotic use regulations in Chinese livestock production, ST398, due to its robust colonization potential, is likely to replace ST9 as the dominant LA-MRSA clone gradually.IMPORTANCELivestock-associated methicillin-resistant (LA-MRSA) is a significant public health concern due to its zoonotic potential and resistance to antimicrobial agents. Despite its global presence, the geographical dominance of specific clones, such as ST398 in Europe and ST9 in Asia, remains poorly understood. This study sheds light on the distinct colonization strategies and metabolic adaptations of these LA-MRSA lineages. By demonstrating the superior colonization abilities and metabolic versatility of ST398 compared to ST9, we speculate that changes in antimicrobial usage policies may drive a shift in the dominance of LA-MRSA clones in China's livestock industry. These insights provide valuable guidance for managing LA-MRSA transmission and developing effective intervention strategies to mitigate its impact on animal and human health.
与家畜相关的耐甲氧西林金黄色葡萄球菌（LA-MRSA）呈现出独特的地理分布模式，ST398在欧洲占主导地位，而ST9是亚洲（尤其是中国）的主要谱系。然而，这些差异背后的机制仍知之甚少。在本研究中，我们评估了从中国和德国分离出的ST9和ST398菌株的细胞黏附能力、抗吞噬特性及猪鼻腔定植潜力。利用16S rRNA基因测序和宏转录组分析进一步探究了定植动态和特征。我们的研究结果显示，LA-MRSA ST398菌株表现出更强的定植能力，包括增强的细胞黏附、对巨噬细胞介导杀伤的抗性增加以及对鼻腔微生物群稳定性的更强影响。定植期间的转录组分析表明，ST398菌株优先利用与基因组修复和氨基酸代谢相关的途径，而ST9菌株，尤其是从中国分离出的菌株，则侧重于碳水化合物代谢。尽管ST9菌株的定植能力相对较弱，但流行的中国ST9分离株携带多个耐药基因[，（L）和（E）-（B）]，对包括泰乐菌素、氟苯尼考和四环素在内的临床重要抗生素表现出广泛耐药性。这表明它们在中国的流行可能通过抗菌选择压力得以维持。随着中国家畜生产中更严格的抗生素使用规定的实施，由于其强大的定植潜力，ST398可能会逐渐取代ST9成为主要的LA-MRSA克隆。
重要性
与家畜相关的耐甲氧西林金黄色葡萄球菌（LA-MRSA）因其人畜共患病潜力和对抗菌剂的耐药性而成为重大公共卫生问题。尽管它在全球都有存在，但特定克隆的地理优势，如欧洲的ST398和亚洲的ST9，仍了解甚少。本研究揭示了这些LA-MRSA谱系独特的定植策略和代谢适应性。通过证明ST398与ST9相比具有更强的定植能力和代谢多样性，我们推测抗菌药物使用政策的变化可能会推动中国家畜行业中LA-MRSA克隆优势的转变。这些见解为管理LA-MRSA传播和制定有效的干预策略以减轻其对动物和人类健康的影响提供了有价值的指导。
