Effects of integrated multi-trophic aquaculture on microbial communities, antibiotic resistance genes, and cultured species: A case study of four mariculture systems

Abstract

Aquaculture is an important protein source in many countries, including China. Integrated multitrophic aquaculture (IMTA) is widely used to reduce the environmental pressure of aquaculture and to increase profits. However, effects of IMTA on host immune and metabolic responses, the dynamics of bacterial communities, and antibiotic resistance genes (ARGs) are relatively understudied. In this study, the IMTA mariculture systems with different combinations of the hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂), the whiteleg shrimp (Litopenaeus vannamei), and the alga (Gracilaria bailinae) were constructed to evaluate the effects of different culture systems on the aquatic environment and cultured species during the initial stage of aquaculture. Results showed that G. bailinae could effectively remove inorganic nutrients accumulated in water, which in turn significantly promoted growth and enhanced non-specific immunity and glycolipid metabolism in the hybrid grouper. Although ARGs were present throughout the culture process, the relative abundance of ARGs in three of the four culture systems decreased with culture time. This was especially the case in the monoculture and the fish-algal IMTA systems, indicating that these aquaculture systems had a scavenging effect on ARGs in the environment. Correlation and network analyses indicated that ARGs were not significantly correlated with environmental factors but were closely related to bacterial communities. Approximately 25 bacterial groups of Bacteroidetes and Proteobacteria were significantly correlated with ARGs, including aminoglycoside, beta-lactamase, chloramphenicol, and multidrug resistance genes. Moreover, tnpA-07, a transposase gene, indirectly affected ARGs through its interaction with Acteroidetes and Proteobacteria. This study provides insights into further optimizing culture methods and controlling the spread and ecological risk of ARGs in IMTA systems.