Combined intestinal transcriptome and microbiome profiling highlights microbiota involved in growth and immunity of the Reeves’ turtle (Mauremys reevesii)

The intestine serves as the primary digestive and essential mucosal immune organ, harboring diverse microbiota that play crucial roles in digestion, absorption, and host immunity. However, the association between the intestinal microbiota and host growth and immunity remains insufficiently established, particularly in ectothermic animals where microbiota are easily influenced by external environments. Herein, a comparative analysis of histology, gene expression, transcriptome, and microbiome was deployed to systematically investigate the potential relevance of growth traits, immune responses, and gut microbiota between Reeves' turtles with inferior (IGP) or superior growth performance (SGP). Our results revealed that, in comparison to the IGP group, the SGP group exhibited histological intestinal structures that were more conducive to digestion and absorption, thereby aligning with its superior growth traits. Moreover, transcriptomic annotation identified 50 differentially expressed genes (DEGs) associated with growth and 70 DEGs involved in immunity. These DEGs showed significant enrichment in growth- and immunity-related GO terms and KEGG pathways. Further RT-PCR analyses validated the expression profiles of several genes related to growth and immunity across multiple tissues. In addition, analysis of microbial abundance revealed the presence of various sensitive indicator genera, such as Lactobacillus and Brevundimonas, which potentially imply host growth performance and immune response. At the phylum level, a more diverse and stable microbial interaction between intestinal microbiota in the SGP group and aquaculture water was predicted to contribute to superior growth performance and immunity. Furthermore, correlation analyses revealed a potential interplay between indicator genera with DEGs associated with growth and immune responses. Taken together, these findings highlight the intricate interplay of intestinal microbiota, environmental microbiota, as well as growth- and immunity-related genes in shaping host traits, providing valuable insights into promoting healthy culture practices for Reeves’ turtles from both molecular and microbiological perspectives.