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Anim Microbiome
2023 Oct 24;51:54. doi: 10.1186/s42523-023-00276-2.
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Unveiling the early life core microbiome of the sea cucumber Apostichopus japonicus and the unexpected abundance of the growth-promoting Sulfitobacter.
Yu J
,
Jiang C
,
Yamano R
,
Koike S
,
Sakai Y
,
Mino S
,
Sawabe T
.
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BACKGROUND: Microbiome in early life has long-term effects on the host's immunological and physiological development and its disturbance is known to trigger various diseases in host Deuterostome animals. The sea cucumber Apostichopus japonicus is one of the most valuable marine Deuterostome invertebrates in Asia and a model animal in regeneration studies. To understand factors that impact on host development and holobiont maintenance, host-microbiome association has been actively studied in the last decade. However, we currently lack knowledge of early life core microbiome during its ontogenesis and how it benefits the host's growth.
RESULTS: We analyzed the microbial community in 28 sea cucumber samples from a laboratory breeding system, designed to replicate aquaculture environments, across six developmental stages (fertilized eggs to the juvenile stage) over a three years-period to examine the microbiomes' dynamics and stability. Microbiome shifts occurred during sea cucumber larval ontogenesis in every case. Application of the most sophisticated core microbiome extraction methodology, a hybrid approach with abundance-occupancy core microbiome analyses (top 75% of total reads and > 70% occupation) and core index calculation, first revealed early life core microbiome consisted of Alteromonadaceae and Rhodobacteraceae, as well as a stage core microbiome consisting of pioneer core microbe Pseudoalteromonadaceae in A. japonicus, suggesting a stepwise establishment of microbiome related to ontogenesis and feeding behavior in A. japonicus. More interestingly, four ASVs affiliated to Alteromonadaceae and Rhodobacteraceae were extracted as early life core microbiome. One of the ASV (ASV0007) was affiliated to the Sulfitobactor strain BL28 (Rhodobacteraceae), isolated from blastula larvae in the 2019 raring batch. Unexpectedly, a bioassay revealed the BL28 strain retains a host growth-promoting ability. Further meta-pangenomics approach revealed the BL28 genome reads were abundant in the metagenomic sequence pool, in particular, in that of post-gut development in early life stages of A. japonicus.
CONCLUSION: Repeated rearing efforts of A. japonicus using laboratory aquaculture replicating aquaculture environments and hybrid core microbiome extraction approach first revealed particular ASVs affiliated to Alteromonadaceae and Rhodobacteraceae as the A. japonicus early life core microbiome. Further bioassay revealed the growth promoting ability to the host sea cucumber in one of the core microbes, the Sulfitobactor strain BL28 identified as ASV0007. Genome reads of the BL28 were abundant in post-gut development of A. japonicus, which makes us consider effective probiotic uses of those core microbiome for sea cucumber resource production and conservation. The study also emphasizes the importance of the core microbiome in influencing early life stages in marine invertebrates. Understanding these dynamics could offer pathways to improve growth, immunity, and disease resistance in marine invertebrates.
Fig. 1. Alpha and beta diversity among sea cucumber samples. a Box-plot based on evenness index (Kruskal-Wallis, p < 0.05). b Unweighted UniFrac distance plot between sea cucumber larvae at different developmental stage (PERMANOVA, p < 0.05, q < 0.05). FE: Fertilized Egg; GL: Gastrula; EA: Early Auricularia; LA: Late Auricularia; PT: Pentactula; JN: Juvenile. c PCoA plot based on Bray–Curtis distance and d PCoA plot based on Unweighted UniFrac distance. Different colors represent different years; closed circles represent larvae samples before gut development, triangles represent larvae samples post gut development. e NMDS (non-metric multidimensional scaling) ordination based on Bray–Curtis distance showing the differences of microbiome both pre and post gut development. preGD: pre gut development; postGD: post gut development. f NMDS ordination based on Bray–Curtis distance showing the differences of microbiome between years. g Unweighted UniFrac distance plot between different years ((PERMANOVA, p = 0.001, q < 0.05) and h Unweighted Unifrac distance plot between sea cucumber larvae before and post gut development (PERMANOVA, p = 0.001, q < 0.05)
Fig. 2. The linear discriminant analysis effect size (LEfSe) analysis of microbial abundance among sea cucumber larvae samples at different developmental stage. a Taxa until order level with significant differences pre- and post-gut development were detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05. b The cladogram of detected prokaryotic taxa for microbial community pre- and post-gut development. c Only family level taxa with significant differences pre- and post-gut development were detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05. d Only family level taxa with significant differences at each developmental stage were detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05. e Only genus level taxa with significant differences at each developmental stage were detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05
Fig. 3. Family-level taxonomic distribution among sea cucumber and seawater samples. a Family-level taxonomic distribution among sea cucumber larvae at different developmental stage. Bars represent the relative percentage of each bacterial family. FE: Fertilized Egg; GL: Gastrula; EA: Early Auricularia; LA: Late Auricularia; PT: Pentactula; JN: Juvenile. b Family-level taxonomic distribution among rearing seawater of sea cucumber larvae at different developmental stage. FESW: Fertilized egg rearing seawater; GLSW: Gastrula rearing seawater; EASW: Early Auricularia rearing seawater; LASW: Late Auricularia rearing seawater; PTSW: Pentactula rearing seawater; JNSW: Juvenile rearing seawater
Fig. 4. Microbiota shared within sea cucumber and seawater samples. a Venn diagram depicting unique and shared bacteria orders and families among sea cucumber larvae and their rearing seawater. b Boxplot based on unweighted UniFrac distance of atrophy larvae and their rearing seawater (PERMANOVA, p < 0.05, q < 0.05). Scale represents similarity within samples. c PCoA plot based on Unweighted UniFrac distance. Colors represent different developmental stages. Closed circles represent larvae samples and open circles represent seawater samples. d NMDS ordination based on Bray-Curtis distance showing the differences of microbiome between sea cucumber larvae and seawater
Fig. 5. The linear discriminant analysis effect size (LEfSe) analysis of microbial abundance among sea cucumber larvae samples and their rearing seawater. a Taxa with significant differences in larvae and rearing seawater were detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05. b The cladogram of detected prokaryotic taxa for microbial community of larvae and rearing seawater. c Only family level taxa with significant differences in larvae and rearing seawater detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05. d Taxa with significant differences in rearing seawater pre- and post-gut development were detected by LEfSe analysis with a LDA threshold score of 3.5 and a p-value of 0.05
Fig. 6. Detection of early life core microbiome and stage core microbiome. a Heatmap of core microbiome and stage core microbiome. Scale represents relative abundance. Scale represents relative abundance. Legend bar shows the sample developmental stage and gut development status. Stage shows the samples collected from different developmental stage. Dark yellow: fertilized egg, purple: gastrula, turquoise: early auricularia, dark green: late auricularia, pink: pentactula, and blue: juvenile, respectively. GutDev shows the gut development status of samples, light yellow represents samples before gut developed and light green represents samples post gut developed. FE: Fertilized Egg; GL: Gastrula; EA: Early Auricularia; LA: Late Auricularia; PT: Pentactula; JN: Juvenile. GutDev shows the gut development status of samples, light yellow represents samples before the gut developed and light green represents samples post-gut development. b CI for core bacteria (at the family level) in the sea cucumber larvae and NorCI, the normalized core index
Fig. 7. Growth promoting ability of Sulfitobacter sp. BL28. a A phylogenetic tree based on ASVs having > 500 reads with relative abundance. Inner circles represent taxonomic analysis at genus level. Red colored heatmap represent relative abundance of ASVs in sea cucumber samples. FE: Fertilized egg; GL: Gastrula; EA: Early auricularia; LA: Late auricularia; PT: Pentactula; JN: Juvenile. Star represents the key feature at different developmental stage. Red: fertilized egg; yellow: stages before gut developed; green: late auricularia; purple: stages post gut development; orange: Sulfitobacter. b Growth performance of juvenile sea cucumber with diet supplementary BL28. Bayes t-test with independent samples was performed using the JASP version 0.17.0 and growth with BL28 > those of control was set as an alternative hypothesis (H1), respectively. Alternative hypothesis was more likely to be occurred by 655 folds, respectively (n = 15). The error bar indicates standard error
Fig. 8. Meta-pangenomic analysis of Sulfitobacter sp. reveals its coverage in microbiota before and post gut development. a Pangenomics of Sulfitobacter sp. indicated the unique and core genes in BL28, and the higher total genome coverage in the post gut development. The inner radial dendrogram shows the gene clusters in the pangenome, clustered by presence/absence across genomes. The four genomes of Sulfitobacter strains are plotted on the innermost four layers, spaced to reflect discernable groups based on genomic composition. The genome pointed in orange is BL28 isolated from sea cucumber microbiome. Gene clusters within a given genome are filled in with black or dark orange; gene clusters do not present remain unfilled or light orange. Core gene across the Sulfitobacter strains were pointed in red and unique gene detected in BL28 were pointed in orange. Above the genome content summaries, each genome’s median coverage across larval metagenomes with different gut development status is shown in the colored bar graph. ANI value of genome is shown in the heatmap above, where each row represents a different sample, and cell color intensity reflects the ANI value. The colored two layers show the proportion of genes within each gene cluster determined to be environmental accessory or core genes: EAGs (green) and ECGs (blue) with 23 metagenomes. b Mean coverage of each gene in the pangenome of Sulfitobacter sp. within two developments indicated higher coverage in metagenomes of post-gut development environment. Outer layers show the four genomes of Sulfitobacter spp.and the coverage in environmental metagenomes. PGD, post gut development; BGD, before gut development
Fig. 9. Microbial function analysis of larvae among different developmental stages. a Distribution of microbial functions among larvae samples before and post gut developed. Bars represent the relative percentage of each microbial functions. b Dynamics of significantly changed microbial functions pre- and post-gut development. Scale represents relative abundance. Legend bar shows the sample developmental stage and gut development status. Stage shows the samples collected from different developmental stages. Dark yellow: fertilized egg, purple: gastrula, turquoise: early auricularia, dark green: late auricularia, pink: pentactula, and blue: juvenile, respectively. GutDev shows the gut development status of samples, light yellow represents samples before gut developed and light green represents samples post gut developed
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