Saha Shouvik, Xiong Jiu-Qiang, Patil Swapnil M, Ha Geon-Soo, Hoh Jeong-Kyu, Park Hyun-Kyung, Chung Woojin, Chang Soon Woong, Khan Moonis Ali, Park Ho Bum, Jeon Byong-Hun
Natural Resources Research Institute, University of Minnesota Duluth, Duluth, MN 55812, USA; Department of Earth Resources and Environmental Engineering, Hanyang University, Seoul 04763, the Republic of Korea.
College of Marine Life Sciences, Ocean University of China, Qingdao 266003, Shandong, China.
J Hazard Mater. 2023 Jun 15;452:131200. doi: 10.1016/j.jhazmat.2023.131200. Epub 2023 Mar 12.
The preeminence of sulfonamide drug resistance genes in food waste (FW) and the increased utilization of high-strength organic FW in anaerobic digestion (AD) to enhance methane production have raised severe public health concerns in wastewater treatment plants worldwide. In this regard, the dissemination patterns of different sulfonamide resistance genes (sul1 and sul2) and their impact on the digester core microbiota during AD of FW leachate (FWL) were evaluated. The presence of various sulfonamide antibiotics (SAs) in FWL digesters improved the final methane yield by 37 % during AD compared with FWL digesters without SAs. Microbial population shifts towards hydrolytic, acidogenic, and acetogenic bacteria in the phyla Actinobacteriota, Bacteroidota, Chloroflexi, Firmicutes, Proteobacteria, and Synergistota occurred due to SA induced substrate digestion and absorption through active transport; butanoate, propanoate, and pyruvate metabolism; glycolysis; gluconeogenesis; the citrate cycle; and pentose phosphate pathway. The initial dominance of Methanosaeta (89-96 %) declined to 47-53 % as AD progressed and shifted towards Methanosarcina (40 %) in digesters with the highest SA concentrations at the end of AD. Dissemination of sul1 depended on class 1 integron gene (intl1)-based horizontal gene transfer to pathogenic members of Chloroflexi, Firmicutes, and Patescibacteria, whereas sul2 was transmitted to Synergistota independent of intl1. Low susceptibility and ability to utilize SAs during methanogenesis shielded methanogenic archaea against selection pressure, thus preventing them from interacting with sul or intl1 genes, thereby minimizing the risk of antibiotic resistance development. The observed emergence of cationic antimicrobial peptide, vancomycin, and β-lactam resistance in the core microbiota during AD of FWL in the presence of SAs suggests that multidrug resistance caused by bacterial transformation could lead to an increase in the environmental resistome through wastewater sludge treatment.
磺胺类耐药基因在食物垃圾（FW）中的优势地位，以及在厌氧消化（AD）中高强度有机FW用于提高甲烷产量的利用率不断增加，引发了全球污水处理厂对公众健康的严重担忧。在这方面，评估了不同磺胺类耐药基因（sul1和sul2）在FW渗滤液（FWL）厌氧消化过程中的传播模式及其对消化池核心微生物群的影响。与不含磺胺类药物的FWL消化池相比，FWL消化池中各种磺胺类抗生素（SAs）的存在使厌氧消化过程中的最终甲烷产量提高了37%。由于SA通过主动运输诱导底物消化和吸收，导致微生物种群向放线菌门、拟杆菌门、绿弯菌门、厚壁菌门、变形菌门和互养菌门中的水解菌、产酸菌和产乙酸菌转变；丁酸、丙酸和丙酮酸代谢；糖酵解；糖异生；柠檬酸循环；以及磷酸戊糖途径。随着厌氧消化的进行，甲烷八叠球菌的初始优势地位（89-96%）下降至47-53%，在厌氧消化结束时SA浓度最高的消化池中，向甲烷鬃毛菌转变（40%）。sul1的传播依赖于基于1类整合子基因（intl1）的水平基因转移，转移到绿弯菌门、厚壁菌门和Patescibacteria的致病成员中，而sul2独立于intl1传播到互养菌门。产甲烷古菌在产甲烷过程中对SAs的低敏感性和利用能力使其免受选择压力，从而防止它们与sul或intl1基因相互作用，从而将抗生素耐药性发展的风险降至最低。在存在SAs的情况下，FWL厌氧消化过程中核心微生物群中观察到阳离子抗菌肽、万古霉素和β-内酰胺耐药性的出现，这表明细菌转化引起的多重耐药性可能通过废水污泥处理导致环境抗性组增加。
