Sustainability of the rice-crayfish co-culture aquaculture model: microbiome profiles based on multi-kingdom analyses

Abstract

While the rice-crayfish culture (RCFP) model, an important aquaculture model in Asia, is generally considered a sustainable model, its sustainability in terms of microbial community profiles has not been evaluated. In this study, multi-kingdom analyses of microbiome profiles (i.e., bacteria, archaea, viruses, and eukaryotes) were performed using environmental (i.e., water and sediment) and animal gut (i.e., crayfish and crab gut) microbial samples from the RCFP and other aquaculture models, including the crab-crayfish co-culture, crayfish culture, and crab culture models, to evaluate the sustainability of the RCFP systematically. Results showed that RCFP samples are enriched with a distinct set of microbes, including Shewanella, Ferroplasma, Leishmania, and Siphoviridae, when compared with other aquaculture models. Additionally, most microbes in the RCFP samples, especially microbes from different kingdoms, were densely and positively connected, which indicates their robustness against environmental stress. Whereas microbes in different aquaculture models demonstrated moderate levels of horizontal gene transfer (HGT) across kingdoms, the RCFP showed relatively lower frequencies of HGT events, especially those involving antibiotic resistance genes. Finally, environmental factors, including pH, oxidation–reduction potential, temperature, and total nitrogen, contributed profoundly to shaping the microbial communities in these aquaculture models. Interestingly, compared with other models, the microbial communities of the RCFP model were less influenced by these environmental factors, which suggests that microbes in the latter have stronger ability to resist environmental stress. The findings collectively reflect the unique multi-kingdom microbial patterns of the RCFP model and suggest that this model is a sustainable model from the perspective of microbiome profiles.

Microbial biogeochemical cycling reveals the sustainability of the rice-crayfish co-culture model

“…Though the ammonium was transformed to organ N under gltB genes ( Figure 2 B), the organ N was significantly converted into ammonium by gdh2 gene (p < 0.1), which resulted in the accumulation of ammonium in non-RCFP ( Figure S1 E). The higher organic decomposition abilities in non-RCFP might be caused by the higher fertilizer inputs in non-RCFP, 16 , 20 which was also supported by our analyzed data ( Figures S1 C–S1F). These phenomena were also observed in sediment ( Figure 2 C) and crayfish gut habitats ( Figure 2 D).…”

“… 20 , 22 , 24 , 25 Comparing the microbial communities of RCFP and other aquaculture models revealed that the RCFP aquaculture model possesses a distinct set of microbes, robust microbial community, lower ARG content, and HGT events, and is less affected by environmental factors. 16 , 26 , 27 All of these findings have demonstrated the sustainability of the rice-crayfish aquaculture model. However, as major drivers of biogeochemical cycling, 28 , 29 there lacks of research on analyzing the role of microbiome in biogeochemical cycling between the RCFP and non-RCFP, which hinders our deeper understanding of the sustainability of RCFP from the perspective of microbial biogeochemical cycling.…”

“… 36 , 37 As important members of ecosystems, microbial biogeochemical cycles contribute profoundly to these processes. While rice-crayfish co-culture model has been implemented at the largest scale in China due to its high productivity and low environmental impact, 16 , 19 , 20 , 22 , 23 , 26 the underline microbial biogeochemical cycles remain uncharted. A few previous research studies have reported the potential role of the microbiome in biogeochemical cycling in natural marine and freshwater ecosystems, 8 , 10 , 38 , 39 while fewer studies have explored the microbial community, functions, and metabolic pathways involved in biogeochemical cycling in an engineered ecosystem, such as RCFP aquaculture model.…”

“…To balance high productivity and environmental sustainability, 16 different aquaculture models have been developed, especially the co-culture models, which are important forms of aquaculture due to their high productivity and lower environmental pollution. 17 , 18 , 19 In recent years, rice-crayfish co-culture model (RCFP) is widely implemented in China due to its eco-friendliness.…”

Probiotics, Prebiotics, and Synbiotics Utilization in Crayfish Aquaculture and Factors Affecting Gut Microbiota

“…Generally, in rice–crayfish culture, enriched microbes in crayfish gut from distinct sets are observed, which include Shewanella , Ferroplasma , Leishmania , and Siphoviridae genera [ 130 ]. Further, in rice co-culture fields, beneficial bacterial taxa, including Bacillus sp., Streptomyces sp., Lactobacillus sp., Prevotella sp., Rhodobacter sp., Bifidobacterium sp., Akkermansia sp., and Lactococcus sp., have been identified, while opportunistic pathogens, ( Citrobacter sp., Aeromonas sp.)…”