A comparative analysis of the gut microbiome and immune gene expression in two Penaeus monodon populations

Abstract

Maintaining intestinal homeostasis is important for shrimp health in aquaculture, particularly under the constant exposure to environmental and biological stressors. While much research has focused on disease-related dysbiosis, the fundamental mechanisms of homeostasis under normal conditions remain largely uncharacterized. To address this gap, postlarval black tiger shrimp (Penaeus monodon) from two distinct genetic lineages, domestic and imported broodstock, were reared in a shared aquaculture environment for three months to observe baseline interaction between intestinal microbiota and immune responses. Intestinal microbiota was examined using 16S rRNA gene (V3-V4) sequencing, and transcriptomic profiles of the intestines were analyzed using RNA sequencing. Average final weight was not significantly different (p = 0.66) between two sources. Microbiota from the intestines of shrimp from different sources showed significant differences at all sampling periods throughout the feeding trial (p < 0.05), based on PERMANOVA results. Vibrio, Colwellia, Pseudoalteromonas, Shewanella, and Tenacibaculum were the dominant bacterial genera in the intestines of shrimp from both groups. Several discriminant genera between the two groups were also identified, including Pseudoalteromonas, Mesoflavibacter, Maribacter, Spongiimonas, Desulfobulbus, and uncultured JGI o_JGI 0000069-P22 (Patescibacteria group). Transcriptomic analysis revealed that while both groups expressed immune-related genes across broad functional categories like pattern recognition proteins (PRPs), proteinase and protease inhibitors (PPIs), and antimicrobial peptides (AMPs), they appeared to employ different sets of individual genes or isoforms within these functional groups. These findings suggest that shrimp's immune systems during normal conditions can utilize different pathways within the same functional categories to control the intestinal microbiome. The pathways preference could be due to their genetic background and baseline microbiota. A better understanding of the unstressed host-microbiota interaction could help guide the microbiome management strategies to maintain gut homeostasis for sustainable disease control in shrimp aquaculture.

Keywords: Genetic influence; Host-gut microbial relationship; Immune homeostasis; Microbiome; Penaeus monodon; Transcriptome.