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Spiculogenesis and biomineralization in early sponge animals - PubMed

  • ️Tue Jan 01 2019

Spiculogenesis and biomineralization in early sponge animals

Qing Tang et al. Nat Commun. 2019.

Abstract

Most sponges have biomineralized spicules. Molecular clocks indicate sponge classes diverged in the Cryogenian, but the oldest spicules are Cambrian in age. Therefore, sponges either evolved spiculogenesis long after their divergences or Precambrian spicules were not amenable to fossilization. The former hypothesis predicts independent origins of spicules among sponge classes and presence of transitional forms with weakly biomineralized spicules, but this prediction has not been tested using paleontological data. Here, we report an early Cambrian sponge that, like several other early Paleozoic sponges, had weakly biomineralized and hexactine-based siliceous spicules with large axial filaments and high organic proportions. This material, along with Ediacaran microfossils containing putative non-biomineralized axial filaments, suggests that Precambrian sponges may have had weakly biomineralized spicules or lacked them altogether, hence their poor record. This work provides a new search image for Precambrian sponge fossils, which are critical to resolving the origin of sponge spiculogenesis and biomineralization.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1

Vasispongia delicata Tang and Xiao, n. gen. & sp. from the Hetang Formation. a–c Carbonaceous compressions of sponge body fossils. Yellow and green arrows bracket putative osculum and spongocoel, respectively. Polygonal cracks in a are manifested as black in color. VPIGM-4699 (16-HT-T6-1-1), VPIGM-4700 (16-HT-T5-6-1), and VPIGM-4701 (16-HT-T3-77-1), respectively. d−j Demineralized spicules. d and g are magnifications of rectangles in a and f, respectively. Blue arrows in h and j point to protuberances or aborted rays. e, f VPIGM-4702 and VPIGM-4703, respectively; h–j VPIGM-4704, VPIGM-4705, and VPIGM-4706, respectively. Honeycomb-like structures (d, e, i, j) in the carbonaceous matrix are molds of framboidal pyrite. a–c are reflected light micrographs (RLM) and h is backscattered electron scanning electron microscopy (BSE-SEM) micrograph. All other images in this and other figures are secondary electron scanning electron microscopy (SE-SEM) micrographs unless otherwise noted. ic inner core, ot outer lamella

Fig. 2
Fig. 2

Demineralized spicules of Vasispongia delicata. a–d Cross-sectional views of spicules with inner core and outer lamella. VPIGM-4707, VPIGM-4708, and VPIGM-4709, respectively. d is a magnification of the rectangle in c. e, f Lateral views of axial filaments. VPIGM-4710 and VPIGM-4711, respectively. g, h Magnifications of white and yellow rectangles in f, respectively. cs cylindrical structure, ot outer lamella, ic inner core

Fig. 3
Fig. 3

Cylindrical structures of Vasispongia delicata, showing concentrically arranged inner core and outer lamella. a, b Cross-sectional views. VPIGM-4712 and VPIGM-4713, respectively. c, f, g Lateral views. VPIGM-4714, VPIGM-4715, and VPIGM-4716, respectively. d, h Magnifications of the yellow frames in c and g, respectively, showing well-preserved outer lamellae. e, i Magnifications of the blue frames in c and g, respectively, showing partially degraded outer lamellae. ic inner core, ot outer lamella. Honeycomb-like structures (a–d, f–i) in the carbonaceous matrix are molds of framboidal pyrite

Fig. 4
Fig. 4

Preservation of organic and biosilica structures in Vasispongia delicata. a Demineralized spicule. VPIGM-4717. b EDS point analysis and element maps of a. c BSE-SEM micrograph of partially demineralized spicule. VPIGM-4718. d EDS point analysis and element maps of c, showing organic axial filament enveloped by a silica lamella. Colored dots in a and c denote the location of EDS point analyses shown in b and d, respectively. ic inner core, ot outer lamella, SiO2 siliceous layer

Fig. 5
Fig. 5

Spiculogenesis and morphological reconstruction of early sponges. Schematic reconstructions of early sponges with weakly biomineralized spicules and entirely organic skeletons as inferred from Vasispongia delicata. Pattern of spicule/skeleton distribution and orientation is conjectural but based on Cambrian reticulosan sponges. Organic skeletons and weakly biomineralized spicules in the sponge body reconstruction are colored in black and orange, respectively. af axial filament, ol organic layer, SiO2 siliceous layer

Fig. 6
Fig. 6

Relative organic proportion in fossil and extant sponge spicules. a Plot of organic proportion measurements of fossil and extant sponge spicules. Organic proportion of sponge spicules was estimated as the relative thickness of combined organic structures (including axial filament, organic layer, and outer sheath) in spicules. When axial filaments are not preserved, axial canals were measured as a maximum estimates of axial filament size. Data based on axial filament measurements are plotted with box and whiskers, where box represents 25–75th percentiles, bar within box represents 50th precentile, and whiskers represent 1.5 × IQR (interquartile range) extensions from the box up to minimum and maximum measurements, with outliers plotted beyond whiskers. See Supplementary Data 1 and 2 for data. b Mean and 95% confidence interval calculated from a subsampling analysis with data binned by geological periods and subsampled 10,000 times, each with six organic proportion measurements (i.e., fewest measurements in any bin). Cm Cambrian, O Ordovician, S Silurian, D Devonian, C Carboniferous, P Permian, TR Triassic, J Jurassic, K Cretaceous, Pg Paleogene, N Neogene, Q Quaternary and extant. Source data are provided as a Source Data file

Fig. 7
Fig. 7

Organic filamentous microstructures preserved in Ediacaran microfossils and axial filaments of extant hexactinellid spicules. a, c Transmitted-light microscopy photographs of phosphatized spherical microfossils in petrographic thin-section obtained from the Ediacaran Doushantuo Formation in South China. Modified from ref. . Arrowheads point to the locations where transverse cross sections (red lines) were prepared across the filamentous microstructures using focus ion beam electron microscopy (FIB-EM). b Bright-field scanning/transmission electron microscopy (TEM) photograph of a microstructure cross-section prepared from a as an ultra-thin foil, showing that the filament is generally rectangular in cross section. The darker polygon is a euhedral apatite crystal that diagenetically intrudes the filament. d SE-SEM micrograph of microstructure cross-section prepared from c, showing a rectangular cross section. e TEM image of the rectangular cross-section of an axial filament in a spicule of the hexactinellid sponge Schaudinnia arctica. Modified from ref. . with permission from author. The slightly lozenge shape of the cross-section is probably due to an oblique section. f SEM micrograph of the square cross section (arrowhead) of an axial filament in a hexactinellid sponge spicule. Modified from ref. . with permission from publisher and author.

Fig. 8
Fig. 8

Phylogenetic interpretations of Vasispongia delicata. The phylogenetic tree is simplified and time-calibrated using molecular clock estimates. It omits eumetazoans and ctenophores so that it stands regardless the monophyly– vs. paraphyly of the poriferans and the phylogenetic placement of the ctenophores,,,. Although a few molecular phylogenetic analyses give spurious support for the paraphyly of the Silicea, most other analyses give decisive support for the monophyly of the Silicea– (a topology adopted here). A cylindrical axial filament is indicated as a plesiomorphy of crown-group siliceans, because it is also present in the Paleozoic sponges Cyathophycus loydelli (possibly a total-group demosponge) and Lenica (possibly a stem-group silicean or a stem-group sponge). It is alternatively possible that a cylindrical axial filament could be an autapomorphy of these sponges. This uncertainty, however, does not affect the main conclusion that early sponges may have had weakly biomineralized sponge spicules, which is inferred from the presence of a significant amount of organic matter in many Paleozoic spicules and juvenile spicules of extant sponges. Blue star denotes the possible age of the demosponge biomarker fossil,. Crown-group classes are denoted by red triangles and their earliest fossil representatives are based on ref. . Dashed line around red triangle indicates the lack of crown-group homoscleromorph fossils in the early Paleozoic. Question marks denote uncertain age constraint or phylogenetic placement of characters. ol organic layer, Si biosilica lamella, os organic sheath, Hex Hexactinellida, Demo Demospongiae, Cal Calcarea, Homo Homoscleromorpha, Cam Cambrian, Ord Ordovician

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