Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing 210095, China.
CNRS, UMR 6553 EcoBio, Université de Rennes, Rennes Cedex 35042, France.
Proc Natl Acad Sci U S A. 2024 Apr 16;121(16):e2318160121. doi: 10.1073/pnas.2318160121. Epub 2024 Apr 10.
Organic carbon availability in soil is crucial for shaping microbial communities, yet, uncertainties persist concerning microbial adaptations to carbon levels and the ensuing ecological and evolutionary consequences. We investigated organic carbon metabolism, antibiotic resistance, and virus-host interactions in soils subjected to 40 y of chemical and organic fertilization that led to contrasting carbon availability: carbon-poor and carbon-rich soils, respectively. Carbon-poor soils drove the enrichment of putative genes involved in organic matter decomposition and exhibited specialization in utilizing complex organic compounds, reflecting scramble competition. This specialization confers a competitive advantage of microbial communities in carbon-poor soils but reduces their buffering capacity in terms of organic carbon metabolisms, making them more vulnerable to environmental fluctuations. Additionally, in carbon-poor soils, viral auxiliary metabolic genes linked to organic carbon metabolism increased host competitiveness and environmental adaptability through a strategy akin to "piggyback the winner." Furthermore, putative antibiotic resistance genes, particularly in low-abundance drug categories, were enriched in carbon-poor soils as an evolutionary consequence of chemical warfare (i.e., interference competition). This raises concerns about the potential dissemination of antibiotic resistance from conventional agriculture that relies on chemical-only fertilization. Consequently, carbon starvation resulting from long-term chemical-only fertilization increases microbial adaptations to competition, underscoring the importance of implementing sustainable agricultural practices to mitigate the emergence and spread of antimicrobial resistance and to increase soil carbon storage.
土壤中有机碳的可利用性对塑造微生物群落至关重要，但对于微生物对碳水平的适应以及随之而来的生态和进化后果，仍存在不确定性。我们研究了在经历 40 年的化学和有机施肥后，土壤中的有机碳代谢、抗生素抗性和病毒-宿主相互作用，这些施肥导致了截然不同的碳可利用性：分别是碳贫瘠和碳丰富的土壤。碳贫瘠的土壤促进了与有机质分解相关的假定基因的富集，并表现出利用复杂有机化合物的专业化，反映了争夺竞争。这种专业化赋予了微生物群落在碳贫瘠土壤中的竞争优势，但降低了它们在有机碳代谢方面的缓冲能力，使它们更容易受到环境波动的影响。此外，在碳贫瘠的土壤中，与有机碳代谢相关的病毒辅助代谢基因通过类似于“搭便车”的策略增加了宿主的竞争力和环境适应性。此外，作为化学战（即干扰竞争）的进化后果，假定的抗生素抗性基因，特别是在低丰度药物类别中，在碳贫瘠的土壤中得到了富集。这引发了人们对依赖于化学肥料的常规农业中抗生素抗性传播的担忧。因此，长期化学肥料施肥导致的碳饥饿增加了微生物对竞争的适应能力，强调了实施可持续农业实践的重要性，以减轻抗菌药物抗性的出现和传播，并增加土壤碳储存。
