ECB-ART-49674
Front Microbiol
2020 Jan 01;11:1697. doi: 10.3389/fmicb.2020.01697.
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Schizasterid Heart Urchins Host Microorganisms in a Digestive Symbiosis of Mesozoic Origin.
Ziegler A
,
Gilligan AM
,
Dillon JG
,
Pernet B
.
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Because of their lifestyles, abundance, and feeding habits, infaunal marine deposit feeders have a significant impact on the ocean floor. As these animals also ingest microorganisms associated with their sediment and seawater diet, their digestive tract usually contains a diverse array of bacteria. However, while most of these microorganisms are transients, some may become part of a resident gut microbiome, in particular when sheltered from the main flow of digesta in specialized gut compartments. Here, we provide an in-depth analysis of the structure and contents of the intestinal caecum (IC), a hindgut diverticulum found exclusively in schizasterid heart urchins (Echinoidea: Spatangoida: Schizasteridae). Based on specimens of Brisaster townsendi, in addition to various other schizasterid taxa, our structural characterization of the IC shows that the organ is a highly specialized gut compartment with unique structural properties. Next generation sequencing shows that the IC contains a microbial population composed predominantly of Bacteroidales, Desulfobacterales, and Spirochaetales. The microbiome of this gut compartment is significantly different in composition and lower in diversity than the microbial population in the sediment-filled main digestive tract. Inferences on the function and evolution of the IC and its microbiome suggest that this symbiosis plays a distinct role in host nutrition and that it evolved at least 66 million years ago during the final phase of the Mesozoic.
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FIGURE 1. Morphology of the intestinal caecum (IC) in Brisaster townsendi. (a) Aspect of a living animal, aboral view; Roman numerals denote ambulacra. (b) Situs of vivisected specimen with aboral part of test and attached gonadal material removed, aboral view. (c–e) Close-up photographs of ICs from three different specimens, aboral views. (f–i) Volume renderings of a μCT dataset with 9.5 μm isotropic voxel resolution: virtual slicing of the renderings in aboral (f) and oral (g) as well as oblique posterior (h) and anterior (i) views. (j) Virtual horizontal section of the dataset at the level of the IC. cc, caecal canal; es, esophagus; gc, gastric caecum; go, gonad; hd, haemal duct; ic, intestinal caecum; in, intestine; me, mesentery; pe, petal; ps, primary siphon; re, rectum; sp, spot; st, stomach; te, test. |
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FIGURE 2. Anatomy and ultrastructure of the intestinal caecum (IC) in Brisaster townsendi. (a) Volume rendering of the IC and adjacent intestine based on a μCT scan with 9.5 μm isotropic voxel resolution, aboral view. (b) Virtual vertical section through the IC. (c) Virtual sagittal section through the IC. (d) Virtual sagittal section through the anterior part of the IC using a μCT dataset with 600 nm isotropic voxel resolution. (e) LM micrograph of a semi-thin section of the intestinal wall. (f) LM micrograph of a semi-thin section of the IC’s wall. (g) LM micrograph of the extracted contents of the IC showing microbial population and ciliate. (h) SEM micrograph of the microbial population inside the IC and the underlying digestive epithelium; the hole in the bacterial mass was artificially made. (i) SEM micrograph of the digestive epithelium lining the interior of the IC showing smaller, rod-shaped bacteria attached to cell apices as well as longer, spiral-shaped taxa free within the lumen. (j) SEM micrograph of the coelomic epithelium lining the exterior of the IC. cc, caecal canal; ce, coelomic epithelium; ci, cilium; cl, ciliate; co, coelomocyte; ct, connective tissue; de, digestive epithelium; fi, fibrocyte; hs, haemal space; ic, intestinal caecum; in, intestine; lu, lumen; me, mesentery; mp, microbial population; mv, microvillus; om, organic mass; rb, rod-shaped bacterium; se, sediment; so, somatocoel; sp, spiral-shaped bacterium. |
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FIGURE 3. Ultrastructure of the intestine and intestinal caecum (IC) in Brisaster townsendi. (a,b) Composite overview images showing a vertical section through the intestinal (a) and the IC’s wall (b). (c–i) Structural features of the IC’s wall. (c) Tiny microvilli at the enterocytes’ apices. (d) Numerous rod-shaped bacteria attached to the digestive epithelium of the IC. (e) Attachment site of rod-shaped bacteria. (f) Pinocytotic vesicles and vacuoles in the apical area of the enterocytes. (g) Glycogen granules near the apex of the enterocytes. (h) Podocyte of the coelomic epithelium with underlying connective tissue and folds of the digestive epithelium. (i) Podocyte’s foot processes bordering the basement membrane with underlying haemal lacunae and striated collagen fibrils. Asterisks denote artificial detachment of the coelothel from the basement membrane. aj, adherens junction; ba, bacterium; bm, basement membrane; cf, collagen fibril; ci, cilium; co, coelomocyte; en, enterocyte; fi, filamentous organism; fp, foot process; gg, glycogen granule; hl, haemal lacuna; ig, iron granule; lu, lumen; mc, myocyte; mf, myofibril; mi, mitochondrion; mv, microvillus; np, nerve plexus; nu, nucleus; po, podocyte; pv, pinocytotic vesicle; sc, squamous cell; sd, slit diaphragm; sf, striated fibril; so, somatocoel; tj, tight junction; va, vacuole. |
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FIGURE 4. Ultrastructural and genomic analyses of the microbial population found inside the intestinal caecum (IC) as well as selected gut compartments of Brisaster townsendi and Abatus cordatus. (a–i) TEM and SEM micrographs showing different bacterial morphotypes found inside the IC of B. townsendi. (j,k) Heatmaps depicting co-occurrence of the most abundant operational taxonomic units (OTUs) across four gut compartments with a minimum OTU frequency of 2,000 in B. townsendi (j) and from ICs with a minimum OTU frequency of 150 in A. cordatus (k); colored scales show relative abundance of taxa across all samples, clusters on the left depict Bray-Curtis metric across samples and on the top depict UPGMA hierarchical clustering, SILVA taxonomic identifications were collapsed to family level (j) and order level (k) or higher if taxonomic classification to those levels was not possible. fi, fimbria; fl, flagellum; gg, glycogen granule; ib, inclusion body; ic, intestinal caecum; in, intestine; re, rectum; st, stomach. |
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FIGURE 5. Microbial diversity in four gut compartments of Brisaster townsendi as well as in the intestinal caecum (IC) of Abatus cordatus. (A) Shannon’s diversity index plot for three main gut compartments and the IC of B. townsendi as well as the IC of A. cordatus; p = 0.004. (B) 3D unweighted UniFrac EMPeror PCoA plot of gut samples from B. townsendi shown in purple (stomach), orange (intestine), blue (IC), and green (rectum) as well as samples from A. cordatus shown in red (IC). |
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FIGURE 6. Absence and presence of the intestinal caecum (IC) in selected schizasterid taxa; all images show results obtained using fixed specimens. (a) Protenaster australis, oral view. (b) Brisaster moseleyi, aboral view. (c) Brisaster owstoni, aboral view. (d) Brisaster townsendi, aboral view. (e) Genicopatagus affinis, aboral view. (f) Pseudabatus nimrodi, aboral view. (g) Schizocosmus abatoides, aboral view. (h) Tripylus excavatus, aboral view of a sliced volume rendering obtained using a contrast-enhanced μCT dataset with 10 μm isotropic voxel resolution. gc, gastric caecum; ic, intestinal caecum; in, intestine; re, rectum. |
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FIGURE 7. Volumetric data on the intestinal caecum (IC) in selected schizasterid taxa. (A) Size series of Brisaster townsendi (N = 24); red dots: IC volume (ICV) vs. test length (TL); black tori: ICV as function of test volume (TV) vs. TL; red line: exponential curve with R2 = 0.823 and Y = 5.491(0.07255*X); black line: least squares regression with p < 0.0001, R2 = 0.418, and Y = 0.01005X + 0.1686. (B) ICV as function of TV in samples from twelve different schizasterid species, including B. townsendi; each data point is shown, and black bars represent mean values for each species. |
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FIGURE 8. Distribution of the intestinal caecum (IC) in the Schizasteridae and inferred timing of the origin of the IC and, by inference, of its microbiome; evolutionary tree of the Schizasteridae constructed by calibrating a cladogram against the known fossil record. Morphology-based phylogeny modified from Stockley et al. (2005) and Stara et al. (2016), stratigraphic data taken from Lambert (1933), Clark (1937), McKinney et al. (1988), Markov (1994), Lindley (2001), and Kroh and Smith (2010). Ca, Campanian; Ce, Cenomanian; Co, Coniacian; Eo, Eocene; Ma, Maastrichtian; Mi, Miocene; mya, million years ago; Ol, Oligocene; P, Pliocene; Pa, Paleocene; Q, Quaternary; S, Santonian; Tu, Turonian. |
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