Metagenomic insights into the rapid recovery mechanisms of prokaryotic community and spread of antibiotic resistance genes after seawater disinfection

Jiaojiao Yan; Xinxu Zhang; Xinyong Shi; Jialin Wu; Ziang Zhou; Yawen Tang; Zhen Bao; Nan Luo; Demin Zhang; Jiong Chen; Huajun Zhang

doi:10.1016/j.watres.2024.122887

Metagenomic insights into the rapid recovery mechanisms of prokaryotic community and spread of antibiotic resistance genes after seawater disinfection

Water Res. 2024 Nov 29:271:122887. doi: 10.1016/j.watres.2024.122887. Online ahead of print.

Authors

Jiaojiao Yan¹, Xinxu Zhang², Xinyong Shi³, Jialin Wu⁴, Ziang Zhou³, Yawen Tang³, Zhen Bao³, Nan Luo³, Demin Zhang⁵, Jiong Chen³, Huajun Zhang⁶

Affiliations

¹ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, 315211, China; Shanghai Treatgut Biotechnology Co., Ltd., Shanghai, 200441, China; Key Laboratory of Aquacultural Biotechnology, Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, 315211, China.
² Archaeal Biology Center, Synthetic Biology Research Center, Shenzhen Key Laboratory of Marine Microbiome Engineering, Key Laboratory of Marine Microbiome Engineering of Guangdong Higher Education Institutes, Institute for Advanced Study, Shenzhen University, Shenzhen, 518060, China; Key Laboratory of Aquacultural Biotechnology, Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, 315211, China.
³ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, 315211, China; Key Laboratory of Aquacultural Biotechnology, Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, 315211, China.
⁴ Ningbo Haiwei Ecological Technology Co., Ltd., Ningbo, 315141, China.
⁵ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, 315211, China; Key Laboratory of Aquacultural Biotechnology, Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, 315211, China. Electronic address: [email protected].
⁶ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, 315211, China; Marine Economic Research Center, Donghai Academy, Ningbo University, Ningbo, 315211, China; Key Laboratory of Aquacultural Biotechnology, Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, 315211, China. Electronic address: [email protected].

PMID: 39637691
DOI: 10.1016/j.watres.2024.122887

Abstract

Disinfectants, such as bleaching powder, are widely employed in marine aquaculture worldwide to control the bacterial pathogens and eliminate antibiotic resistance genes (ARGs). Nevertheless, the rapid recovery of prokaryotic community compositions (PCCs) after disinfection may significantly influence the overall efficacy of disinfection. Presently, little is known about the rapid recovery mechanisms of PCCs and its impact on the removal of ARGs in seawater. In this study, 16S rRNA gene sequencing and metagenomic analysis were used to address the above concerns through simulating the disinfection process in aquaculture. The results showed that recovery of PCCs began within 16 h. The underlying mechanisms of the rapid recovery of PCCs were the synergistic interactions between microbes and the residues of disinfection-resistant bacteria (DRB). Disinfection resistance genes (DRGs) related to efflux pump serve as the primary molecular foundation providing DRB to resist disinfection. Among the 78 annotated ARGs, only 10 ARGs exhibited a significant decrease (P < 0.05) after 72 h, implying the ineffective removal of ARGs by bleaching powder. Furthermore, bacterial co-resistance to disinfectants and antibiotics was observed. Genome analysis of two highly resistant DRB from Pseudomonadaceae revealed that both DRB carried 16 DRGs, aiding the recovery of PCCs and the spread of ARGs. These findings provide novel insights in the mechanisms of the rapid recovery of PCCs and bacterial co-resistance to disinfectants and antibiotics, which can be crucial for the management of pathogens and antibiotic resistance in seawater.

Keywords: Antibiotic resistance genes; Disinfection; Disinfection resistance genes; Metagenome; Prokaryotic community.