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Front Microbiol
2020 Jan 01;11:308. doi: 10.3389/fmicb.2020.00308.
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Characterization of the Gut Microbiota of the Antarctic Heart Urchin (Spatangoida) Abatus agassizii.
Schwob G
,
Cabrol L
,
Poulin E
,
Orlando J
.
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Abatus agassizii is an irregular sea urchin species that inhabits shallow waters of South Georgia and South Shetlands Islands. As a deposit-feeder, A. agassizii nutrition relies on the ingestion of the surrounding sediment in which it lives barely burrowed. Despite the low complexity of its feeding habit, it harbors a long and twice-looped digestive tract suggesting that it may host a complex bacterial community. Here, we characterized the gut microbiota of specimens from two A. agassizii populations at the south of the King George Island in the West Antarctic Peninsula. Using a metabarcoding approach targeting the 16S rRNA gene, we characterized the Abatus microbiota composition and putative functional capacity, evaluating its differentiation among the gut content and the gut tissue in comparison with the external sediment. Additionally, we aimed to define a core gut microbiota between A. agassizii populations to identify potential keystone bacterial taxa. Our results show that the diversity and the composition of the microbiota, at both genetic and predicted functional levels, were mostly driven by the sample type, and to a lesser extent by the population location. Specific bacterial taxa, belonging mostly to Planctomycetacia and Spirochaetia, were differently enriched in the gut content and the gut tissue, respectively. Predictive functional profiles revealed higher abundance of specific pathways, as the sulfur cycle in the gut content and the amino acid metabolism, in the gut tissue. Further, the definition of a core microbiota allowed to obtain evidence of specific localization of bacterial taxa and the identification of potential keystone taxa assigned to the Desulfobacula and Spirochaeta genera as potentially host selected. The ecological relevance of these keystone taxa in the host metabolism is discussed.
FIGURE 1. Relative abundance of bacterial classes in Abatus agassizii gut and external sediment microbiota in Ardley and China sampling sites. Bacterial classes were filtered at >0.5% relative abundance threshold and the average of the replicate abundances are presented for each condition (i.e., for each combination of sites and sample types). Each color represents a distinct bacterial class.
FIGURE 2. Non-metric multidimensional scaling ordination of the bacterial community composition of the Abatus agassizii gut and external sediment microbiota. Colors are assigned to the different sample types. Circles and triangles represent samples from Ardley and China sites, respectively. The arrows represent the variations of the 15 discriminant OTUs most significantly correlated with community ordination (envfit, p < 0.05). The letters indicate the taxonomic identification at the family level of the discriminant OTUs (Ba: Bacteroidetes BD2-2, De: Desulfobacteraceae, Fl: Flavobacteriaceae, Ga: Gammaproteobacteria unclassified, Le: Lentimicrobiaceae, Pi: Pirullulaceae, Rh: Rhodobacteraceae, Sa: Sandaracinaceae, Sp: Spirochaetaceae). Effect of the sample type and the site was tested using permutational multivariate analysis of variance (Adonis test) on Bray–Curtis distance matrix computed from the OTU table (details provided in Supplementary Table S2).
FIGURE 3. Functional differentiation of the bacterial communities from the Abatus agassizii gut microbiota determined using PICRUSt v2.2.0. (A) NMDS ordination of the MetaCyc pathways composition of the external sediment and the Abatus agassizii gut microbiota. Colors are assigned to the different sample types. Circles and triangles represent samples from Ardley and China sites, respectively. Ellipses represent the standard deviation of all points for each sample type, with a confidence interval at 0.95. Strength and significance of sample groupings according to the sample type and the site were tested using permutational multivariate analysis of variance (Adonis test) on Bray–Curtis distance matrix computed from pathways’ abundance table. (B) Details of the top 5 MetaCyc pathways significantly enriched either in the gut tissue or in the gut content. Colors are assigned to the different sample type. Relative abundances and p-values obtained from the two-sided Welch’s test corrected with the Benjamini–Hochberg FDR method are provided. Comparisons with p-values < 0.05 were considered significant.
FIGURE 4. Distinctive sample type specificity of the Abatus agassizii microbiota. (A) Venn diagram of shared and specific OTUs for the three sample types (based on the total OTU table). The number of OTUs in each biological sample type is shown. Dark green, light green and aniseed yellow represent the external sediment, the gut content and the gut tissue, respectively. (B) Ternary plot of OTU compositions. Each circle represents one OTU. The size of each circle represents the relative abundance of the OTU (minimum of 0.5% relative abundance). The position of each circle represents its contribution to the relative total abundance of the biological sample type considered. Dark green, light green and aniseed yellow circles mark OTUs significantly enriched in the gut tissue, in the gut content and in the external sediment, respectively (FDR < 0.05). Gray circles represent OTUs without any significative enrichment. (C) Heatmap of the external, gut content and gut tissue enriched OTUs. Vertical columns represent samples. Horizontal rows represent OTUs (minimum of 0.5% relative abundance). Clustering at the top is computed using Pearson correlation coefficient as distance measurement and Ward agglomeration method. Colors on the left side represent OTU sample type enrichment as previously described.
FIGURE 5. Co-occurrence patterns of bacterial taxa from gut microbiota (content and tissue) of Abatus agassiizi, determined through Co-occurrence Network inference (CoNet v1.1.1) and analyzed using Cytoscape (v3.6.0). Panels (A–D) refer to the Abatus populations of Ardley and China sites, respectively. Networks were built from the 321 OTUs coming from the core China/Ardley only. The networks (A,C) were edited using the Compound Spring Embedder algorithm in Cytoscape. Edges are drawn with red and blue lines representing co-exclusion and co-presence interactions, respectively. Nodes represent the bacterial OTUs and were colored according to their taxonomic affiliations (at the family level). Only OTUs with significant edges are represented. Nodes’ size is scaled on the abundance of the OTU (number of reads). Triangles in the networks indicate the hub taxa, defined as nodes with high centrality (i.e., closeness and betweenness) and high connectivity (i.e., node degree) (B,D).
FIGURE 6. Fit to the neutral model for the gut content (A), the gut tissue (B) and the gut microbiota (content and tissue) (C). Each point represents an OTU and the color indicates its fitting to the neutral model. The predicted occurrence frequency and the 95% confidence interval (CI) around the neutral model prediction are drawn. OTUs that are within the confidence limits are well-predicted in terms of frequency and abundance by the neutral model. OTUs that are above the upper CI limit are over-represented in the samples. OTUs that are below the lower CI limit are under-represented in the samples. (∗) OTUs previously identified as hub taxa in the co-occurrence analysis are highlighted. (D) Percent of OTUs that are within, above and below the 95% confidence limits of the neutral model.
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