Biofloc technology (BFT) is a microbial biotechnology that has shown great potential in water quality control and nutrient re-utilization towards sustainable aquaculture. Carbohydrate addition is the main operation means for the application of BFT; however, we are still unclear how it affects microbial-driven nitrogen (N) transformation and utilization in BFT systems. In this study, autotrophic- and heterotrophic-dominated BFT systems (AS vs. HS) in triplicates were operated by two molasses addition strategies for a 13-week production trial of P. vannamei. Throughout the trial, more amount of bioflocs (in terms of VSS) were produced in HS than in AS. Higher concentrations of NH4+-N, NO2−-N, NO3−-N, TIN and TN while lower concentrations of TON were monitored in AS compared to HS. N budget analysis showed that the harvested shrimp deposited >34.4% of input N; and higher N retention in the final culture water while lower N loss and N discharge from the systems were found in AS compared to HS. Higher efficiencies of gross and feed N utilization were achieved in HS (36.6% and 38.8%) than in AS (34.5% and 34.9%). Metagenomic analysis revealed that abundant and diverse N-cycling microbial communities and functional genes in bioflocs constituted a complete and complex N-cycling network, which was the driving force of N transformation and recycling in the culture water of systems. The lower abundances of nitrifying bacteria and associated genes led to the inhibition of nitrification under high molasses addition in HS, which accounted for the differences in N dynamics, budget and utilization efficiency between AS and HS. Together, a quantitative model of N migration and transformation driven by N-cycling microbial communities of bioflocs was depicted in closed BFT systems for shrimp aquaculture. This study firstly revealed the N-cycling microbiome and functional effects in BFT systems, which provides theoretical and technical foundations for efficient N management in intensive aquaculture.
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