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Microbiologyopen
2021 Nov 01;106:e1250. doi: 10.1002/mbo3.1250.
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Distinct microbiota assembly mechanisms revealed in different reconstruction stages during gut regeneration in the sea cucumber Apostichopus japonicus.
Yu Z
,
Xue Z
,
Liu C
,
Zhang A
,
Fu Q
,
Yang K
,
Zhang F
,
Ran L
.
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Apostichopus japonicus is a useful model for studying organ regeneration, and the gut microbiota is important for host organ regeneration. However, the reconstruction process and the mechanisms of gut microbiota assembly during gut regeneration in sea cucumbers have not been well studied. In the present study, gut regeneration was induced (via evisceration) in A. japonicus, and gut immune responses and bacterial diversity were investigated to reveal gut microbiota assembly and its possible mechanisms during gut regeneration. The results revealed that bacterial community reconstruction involved two stages with distinct assembly mechanisms, where the reconstructed community was initiated from the bacterial consortium in the residual digestive tract and tended to form a novel microbiota in the later stage of reconstruction. Together, the results of immunoenzyme assays, community phylogenetic analysis, and source tracking suggested that the host deterministic process was stronger in the initial stage than in the later stage. The bacterial interactions that occurred were significantly different between the two stages. Positive interactions dominated in the initial stage, while more complex and competitive interactions developed in the later stage. Such a dynamic bacterial community could provide the host with energetic and immune benefits that promote gut regeneration and functional recovery. The results of the present study provide insights into the processes and mechanisms of gut microbiota assembly during intestinal regeneration that are valuable for understanding gut regeneration mechanisms mediated by the microbiota.
FIGURE 1. Diversity of the A. japonicus gut bacterial community at different sampling time points. (a) CPCoA analysis of the bacterial communities in the regenerating guts. (b) Variation in Faith's PD index during the sampling period. (c) Variation in the observed ASV index during the sampling period. (d) Variation in the Chao1 index during the sampling period. (e) Variation in the Pielou index during the sampling period. Different lowercase letters above the error bars indicate significant differences among groups
FIGURE 2. Bacterial community composition at the phylum level in different A. japonicus gut samples during gut regeneration
FIGURE 3. The abundances of bacterial genera at different sampling times. Different lowercase letters above the error bars indicate significant differences among groups
FIGURE 4. Changes in gut immunoenzyme activities (aâd) and correlations of enzyme activities with bacterial community structure during A. japonicus gut regeneration (e). Different lowercase letters above the error bars indicate significant differences among groups
FIGURE 5. Ecological networks of the bacterial communities at different stages of A. japonicus gut regeneration. (a) Network interaction graph for the bacterial communities from 1 to 28 dpe. (b) Network interaction graph for the bacterial communities from 28 to 56 dpe. Each node represents a bacterial genus. The color of each node represents the class of the genus associated with the node. A blue edge indicates a positive interaction between two nodes, whereas a red edge indicates a negative interaction
FIGURE 6. SourceTracker analysis showing the contributions of different source communities to the bacterial communities at different stages of gut regeneration. One asterisk (*) indicates statistical significance (p < 0.05), and two asterisks (**) indicate extreme statistical significance (p < 0.01)
FIGURE 7. Analysis of the ecological processes of the bacterial community at different A. japonicus gut regeneration stages. (a) Changes in ses.MNTD over the gut regeneration period. Different lowercase letters above the error bars indicate significant differences among groups. (b) The partitioning of βSOR (solid line) into βSIM (dotted line) and βSNE (dashed line). (c) The proportions of βSIM and βSNE in βSOR. Lowercase letters above the error bars indicate significant differences in βSIM/βSOR among groups and capital letters indicate significant differences in βSNE/βSOR among groups
FIGURE 8. Schematic summary of the bacterial community dynamics and their controlling factors during bacterial community reconstruction. The red arrow indicates the evisceration of the A. japonicus gut. The red circle highlights the bacterial community in the residual digestive tract. The cyan arrow indicates the lumen formation process in the regenerating gut. The cyan circle highlights the bacterial community in the initial stage of reconstruction. The blue arrow indicates the differentiation and growth processes in the regenerating gut. The blue circle highlights the bacterial community in the later stage of reconstruction
FIGURE A1. Gut regeneration process of A. japonicus. es, esophagus, st, stomach, ai, anterior intestine, mi, middle intestine, pi, posterior intestine, vm, ventral mesentery, dm, dorsal mesentery, cl, cloaca; yellowâcolored area, the tissue collected for microbiota analysis
FIGURE A2. Rarefaction curves of different samples
FIGURE A3. Principal coordinate analysis plot illustrating the variation of the bacterial communities in gut and seawater samples during gut regeneration
FIGURE A4. Ternary plot illustrating the succession and relative abundances of bacterial species. The size of the circle represents the relative abundance of each species, and the color represents species affiliated with different major classes
FIGURE A5.
ZâP plot illustrating the distribution of OTUs based on their topological roles. The horizontal dashed line represents Zi = 2.5, and the vertical dashed line represents Pi = 0.62
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