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Anim Microbiome
2021 Nov 15;31:79. doi: 10.1186/s42523-021-00140-1.
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Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis.
Masasa M
,
Kushmaro A
,
Kramarsky-Winter E
,
Shpigel M
,
Barkan R
,
Golberg A
,
Kribus A
,
Shashar N
,
Guttman L
.
Abstract
BACKGROUND: Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in consequent changes in their gut microbe assemblies and association networks.
METHODS: To ascertain whether such changes are led by specific microbes or limited to a specific region in the gut, we compared the microbial assembly in the three major gut regions of the sea urchin Tripneustes gratilla elatensis when fed a mono-specific algal diet of either Ulva fasciata or Gracilaria conferta, or an algal-free diet. DNA extracts from 5 to 7 individuals from each diet treatment were used for Illumina MiSeq based 16S rRNA gene sequencing (V3-V4 region). Niche breadth of each microbe in the assembly was calculated for identification of core, generalist, specialist, or unique microbes. Network analyzers were used to measure the connectivity of the entire assembly and of each of the microbes within it and whether it altered with a given diet or gut region. Lastly, the predicted metabolic functions of key microbes in the gut were analyzed to evaluate their potential contribution to decomposition of dietary algal polysaccharides.
RESULTS: Sea urchins fed with U. fasciata grew faster and their gut microbiome network was rich in bacterial associations (edges) and networking clusters. Bacteroidetes was the keystone microbe phylum in the gut, with core, generalist, and specialist representatives. A few microbes of this phylum were central hub nodes that maintained community connectivity, while others were driver microbes that led the rewiring of the assembly network based on diet type through changes in their associations and centrality. Niche breadth agreed with microbes' richness in genes for carbohydrate active enzymes and correlated Bacteroidetes specialists to decomposition of specific polysaccharides in the algal diets.
CONCLUSIONS: The dense and well-connected microbial network in the gut of Ulva-fed sea urchins, together with animal's rapid growth, may suggest that this alga was most nutritious among the experimental diets. Our findings expand the knowledge on the gut microbial assembly in T. gratilla elatensis and strengthen the correlation between microbes' generalism or specialism in terms of occurrence in different niches and their metabolic arsenal which may aid host nutrition.
Fig. 1. Richness, diversity and similarity of T. gratilla elatensis GMA under different variables of diet and gut region. Shannon index considering a different diets, b gut regions, or c both variables (n = 51). Box plots represent a level of 95% confidence interval, bar plots represent the standard error, straight lines represent the median, and the black dot represents the mean. Dissimilarity between GMA is demonstrated by non-metric multidimensional scaling (NMDS) based on Bray–Curtis dissimilarities between GMA in different d diets e gut regions, or f both forces (n = 51)
Fig. 2. T. gratilla elatensis GMA composition under different variables of diet and gut region. a Illustration of sea urchin digestive tract (performed using magnetic resonance imaging [49] and image illustrator at https://www.nhm.ac.uk/our-science/data/echinoid-directory) followed by the relative abundance of T. gratilla elatensis gut microbes (Genera) in different gut regions and under each diet (n = 54). b Log-transformed count of bacterial phyla with greatest differences in prevalence under a particular diet, middle line represents median, and whiskers are drawn from the 10th to 90th percentiles (n = 54). c Gut bacterial genera identified as diet-biomarkers in T. gratilla elatensis via Linear discriminant analysis (n = 54)
Fig. 3. a Niche breadth of microbes in sea urchin GMA following the different measured indices of Levin's, Shannon–Weaver, and occurrence. Middle line in box plots represents mean value and whiskers are drawn from the 10th to 90th percentiles. Generalist or specialist microbes are shown at top or lowest decile, respectively (n = 434). b Occurrence and cumulative abundance of each of the microbes in GMA indicates differences of niche breadth and specialization in unique habitats. Each dot represents one microbe with a color indication indicating core, core-generalist, generalist, specialist, unique, or not significant (n = 434)
Fig. 4. Association network of T. gratilla elatensis GMA under different variables of diet and gut region. Association network presenting a the general network (regardless of diet or region), and in different examined niches of diets b
Gracilaria, c Pellet, or d
Ulva; or gut regions e esophagus, f stomach, or g intestine. Diamonds indicate hub nodes and triangles indicate driver nodes. Nodes are colored following annotation at Phyla level. Edge color indicates type of association as either co-occurrence (blue) or co-exclusion (red). h Venn diagrams reveal number of shared or unique associations in networks of different diets or gut regions (n = 54)
Fig. 5. Driver nodes to rewire T. gratilla elatensis GMA association network under different variables of diet and gut region. Driver microbes were extracted from networks using NetShift following significant change in degrees and associated partners. Only nodes that presented significant change as compared to the other two diets or regions were identified as driver microbes. Associations of driver nodes in a different diets or b gut regions. Annotation (genus level) of driver microbes include (upper to lower order): denovo22514 (Spirochaeta2), and denovo28887 (Unassigned) as driver microbes in the Gracilaria-diet network; denovo36058 (Roseimarinus) in the pelleted-diet network; denovo31035 (Candidatus Hepatoplasma) in the Ulva-diet network; denovo6214 (Roseimarinus) in the esophagus network; and denovo14715 (uncultured bacterium of Spirochaetes) in the intestine network. Nodes are colored following annotation at Phyla level (n = 54)
Fig. 6. A heatmap diagram of the variation in content and number of copies of glycoside hydrolase (EC 3.2.1.-) and polysaccharide lyase (EC 4.2.2.-) genes in the genome of the identified key microbes that fell into the determination of core (C), core-generalist (Cg), generalist (G), specialist (S), or unique (U) microbes, and the keystone hub microbes in the microbial networks (H)
