Abstract
Host-intestine microbiota interactions have been widely studied in aquatic animals, but these interactions in the intestine regeneration process of the sea cucumber Apostichopus japonicus have been rarely investigated. To understand how intestine regeneration impacts the developing intestinal microbiome composition and function, we performed a case study to characterize the intestinal microbial composition and functional genes of A. japonicus during intestine regeneration stages. High-throughput 16S rRNA gene sequencing revealed significantly different intestine microbiota compositions in different regeneration stages. The phylogenetic diversity and composition of the intestinal microbiota changed significantly in the early regeneration stage and tended to recover in the end stage. During the regeneration process, the abundance of Bacteroidetes and Rhodobacterales increased significantly. A network analysis revealed that Rhodobacteraceae and Flavobacteriaceae may function as keystone taxa in the intestinal microbial community of A. japonicus during intestine regeneration. Metagenomic analyses of representative samples revealed that the microbiomes of regenerating intestines were enriched in genes facilitating cell proliferation, digestion and immunity. The increased abundance of Bacteroidetes elevated the enrichment of genes associated with carbohydrate utilization. Some functional features in the subsystem category changed in a pattern that was consistent with the changing pattern of microbiota composition during intestine regeneration. Our results revealed that seemingly regular alterations in the intestinal microbiome composition and function are associated with intestine regeneration stages. Intestinal microbiota can increase the abundance of beneficial bacterial members and upregulate related functional genes to adapt to intestine regeneration and reconstruct a stable community structure. This study provides a new insight into the mechanism of the host-microbiota interaction response to organ regeneration.
Highlights
Intestinal microbiome, which exert important influences on a host’s development and tissue physiology, immune regulation, metabolic absorption and so on, have been widely studied in many organisms
During the regeneration process, functional genes responsible for cell growth and death, carbohydrate metabolism, the digestive system and the immune system were upregulated (Supplementary Figure 6), which is in accord with shifts in specific microbial communities. These results suggest that intestinal microbiota can regulate the abundance of beneficial members and related functional genes, which are helpful for microbial community reconstruction and intestine regrowth in A. japonicus during regeneration
We observed large alterations in the abundance of major groups and functional genes; interestingly, these alterations were associated with the intestine regeneration stages
Summary
Intestinal microbiome, which exert important influences on a host’s development and tissue physiology, immune regulation, metabolic absorption and so on, have been widely studied in many organisms. The aforementioned broad-spectrum characteristics of intestinal microbiota define them as integral contributors to the development, growth and physiological health of the sea cucumber A. japonicus. Studies have focused on (i) bacterial community structures in the intestine of A. japonicus (Gao et al, 2014a,b); (ii) the physiological characterization of intestinal bacterial isolates (Zhang et al, 2013; Wang et al, 2015); and (iii) the potential effects of intestinal bacteria on sea cucumber growth. Recent studies have attempted to explain how intestinal microbiota are shaped by external factors, such as probiotics, diet and habitat types (Yang et al, 2015; Qi et al, 2017; Wang et al, 2017; Zhao et al, 2018; Ma et al, 2019). Internal factors of organisms that may contribute to intestinal microbiota modulation have been scarcely explored
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