**1. Introduction**

Antibiotic resistance genes (ARGs) are genes governing the expression of enzymes involved in the degradation or in the chemical modification and subsequent inactivation of antibiotics [1]. The emergence of bacterial strains resistant to many antibiotics could be called into questions when using these antibiotics to fight against infectious diseases [2,3]. In the face of this public health problem, it is necessary to define the elements responsible for the emergence of these multiresistant bacteria.

It has now been established that the environment represents a reservoir of resistant bacteria or ARGs that could be transmissible to humans and animals [4]. The occurrence of ARGs in hospital settings, fish farms, organic waste products, wastewater treatment plants and soils/sediments has also been investigated [5–11]. Many organic waste products are used as fertilizer on agricultural soils [12] and treated wastewater or river water into which they are discharged can be used to irrigate crops [13]. Certain agricultural practices can,

**Citation:** Jia, L.; Liu, H.; Zhao, N.; Deng, Q.; Zhu, C.; Zhang, B. Distribution and Transfer of Antibiotic Resistance Genes in Coastal Aquatic Ecosystems of Bohai Bay. *Water* **2022**, *14*, 938. https:// doi.org/10.3390/w14060938

Academic Editors: François Gagné, Stefano Magni and Valerio Matozzo

Received: 29 January 2022 Accepted: 14 March 2022 Published: 17 March 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

therefore, potentially lead to the environmental dissemination of ARGs and the contamination of animals, crops, soils and water resources [14,15]. For example, previous studies have reported that pond water in fish farms and shrimp farms contained ciprofloxacin, penicillin G, rifampicin and vancomycin-related ARGs [16]. The persistence of ARGs in the soils of fish farms has been strongly compared to the surrounding sediments [6].

Aquatic ecosystems constitute a big reservoir of ARGs. It was previously reported that aquaculture systems have a significant impact on the accumulation and spread of antibiotic-resistant bacteria (ARB) and ARGs in freshwater and sediment [16,17]. Fish may ingest ARB from the aquatic environment for their unique living environments, so the fish intestine would be an optimal niche for conjugal ARG transfer. In previous studies, it was reported that the guts of aquatic animals such as zebrafish contained a high abundance and diversity of bacteria, which indicated them as significant potential recipients of ARGs through horizontal gene transfer (HGT) and was beneficial to the spread of ARGs in water environments [18,19]. Moreover, the unique living environments are able to cause aquatic animals to ingest ARB in water easily [19]. There were some data regarding the abundance and the transfer of ARGs among water, sediment (soil) and organisms in aquatic systems [20,21], but the research topic needs an in-depth study. Here, we discuss the abundance of ARGs in aquaculture environments as well as fish ecosystems and the occurrence of the transfer of ARGs among these micro-systems.

The Chinese tongue sole (*Cynoglossus semilaevis*) is a marine fish species widely spread in the Bohai Sea and cultured in the area; however, not enough attention has been paid to the distributions of ARGs related to this fish till now. Based on the above, this study intends to investigate the different classes of ARGs present in the intestinal tract of *C. semilaevis*, culture water and soils in the same area. We also aimed to investigate the exchange and transfer mechanisms of ARGs between these ecosystems. This work hopes to provide a better understanding of the abundance and dissemination of ARGs in aquatic ecosystems.
