Genome-centric metagenomics provides insights into the core microbial community and functional profiles of biofloc aquaculture.

Abstract

Bioflocs are microbial aggregates that play a pivotal role in shaping animal health, gut microbiota, and water quality in biofloc technology (BFT)-based aquaculture systems. Despite the worldwide application of BFT in aquaculture industries, our comprehension of the community composition and functional potential of the floc-associated microbiota (FAB community; ≥3 µm size fractions) remains rudimentary. Here, we utilized genome-centric metagenomic approach to investigate the FAB community in shrimp aquaculture systems, resulting in the reconstruction of 520 metagenome-assembled genomes (MAGs) spanning both bacterial and archaeal domains. Taxonomic analysis identified Pseudomonadota and Bacteroidota as core community members, with approximately 93% of recovered MAGs unclassified at the species level, indicating a large uncharacterized phylogenetic diversity hidden in the FAB community. Functional annotation of these MAGs unveiled their complex carbohydrate-degrading potential and involvement in carbon, nitrogen, and sulfur metabolisms. Specifically, genomic evidence supported ammonium assimilation, autotrophic nitrification, denitrification, dissimilatory nitrate reduction to ammonia, thiosulfate oxidation, and sulfide oxidation pathways, suggesting the FAB community's versatility for both aerobic and anaerobic metabolisms. Conversely, genes associated with heterotrophic nitrification, anaerobic ammonium oxidation, assimilatory nitrate reduction, and sulfate reduction were undetected. Members of Rhodobacteraceae emerged as the most abundant and metabolically versatile taxa in this intriguing community. Our MAGs compendium is expected to expand the available genome collection from such underexplored aquaculture environments. By elucidating the microbial community structure and metabolic capabilities, this study provides valuable insights into the key biogeochemical processes occurring in biofloc aquacultures and the major microbial contributors driving these processes.

Importance: Biofloc technology has emerged as a sustainable aquaculture approach, utilizing microbial aggregates (bioflocs) to improve water quality and animal health. However, the specific microbial taxa within this intriguing community responsible for these benefits are largely unknown. Compounding this challenge, many bacterial taxa resist laboratory cultivation, hindering taxonomic and genomic analyses. To address these gaps, we employed metagenomic binning approach to recover over 500 microbial genomes from floc-associated microbiota of biofloc aquaculture systems operating in South Korea and China. Through taxonomic and genomic analyses, we deciphered the functional gene content of diverse microbial taxa, shedding light on their potential roles in key biogeochemical processes like nitrogen and sulfur metabolisms. Notably, our findings underscore the taxa-specific contributions of microbes in aquaculture environments, particularly in complex carbon degradation and the removal of toxic substances like ammonia, nitrate, and sulfide.