Arrested in Glass: Actin within Sophisticated Architectures of Biosilica in Sponges

Ehrlich, Hermann; Łuczak, Magdalena; Ziganshin, R. Kh.; Mikšı́k, Ivan; Wysokowski, Marcin; Simon, Paul; Baranowska-Bosiacka, Irena; Kupnicka, Patrycja; Ereskovsky, Alexander; Galli, Roberta; Dyshlovoy, Sergey A.; Fischer, Jonas; Tabachnick, Konstantin R.; Petrenko, Iaroslav; Jesionowski, Teofil; Lubkowska, Anna; Figlerowicz, Marek; Ivanenko, Viatcheslav N.; Summers, Adam P.

doi:10.1002/advs.202105059

Cited by 19 publications

(31 citation statements)

References 60 publications

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“…As it is shown in the present paper, the basic building blocks were spicules consisting of a central proteinaceous axial filament surrounded by alternating concentric interlayers of silica and organic matter. Ehrlich et al (2022) showed that axial filaments inside the spicules are found unbound to the mineralized phase. There are actin-rich axial filaments in microscleres.…”

Section: Discussionmentioning

confidence: 99%

Combined complementary imaging techniques in morphological analysis of Spongilla lacustris (Linnaeus 1759)

Woźnica

Karczewski

Gwiazda

et al. 2023

Limnology & Ocean Methods

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Sponges, like Spongilla lacustris, as filter feeders, play an essential role in water purification in aquatic ecosystems. The body of this demosponge, in general, consists of both organic soft skeleton and a siliceous scaffold. Their construction of the spicule-bundling scaffold as mechanical support for skeletal organic mesohyl seems crucial for filtration efficiency. Understanding the structure of the sponge's biosilica-based scaffold as well as its location within three-dimensional (3D) skeletal construct requires the introduction of effective analytical methods. The investigations focused on the morphology and architecture of skeletal elements of S. lacustris utilizing the combination of X-ray computed microtomography (μCT) and scanning electron microscopy with energy-dispersive X-ray spectroscopy (SEM/EDS). The construction details, surface morphology and chemical composition of the sponge scaffold are presented. μCT provided the reconstructed 3D images of skeleton structures, including longitudinally and transversely oriented bundles of overlapping spicules, forming a ladder-like construction as well as the length, geometric distribution, and the surface of the spicules. Further analyses based on SEM/EDS confirmed the proper identification of the structures and their localization and revealed a high abundance of silicon and a low amount of carbon and oxygen in spicules, high abundance of silicon, carbon and oxygen in layered membranes surrounding the bundles of spicules but predominating carbon in the pinacoderm. Combination of these techniques provides a unique image of the sponge body morphology. Verified set of tools may be used for further analyses of sponge body mechanics.

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Section: Discussionmentioning

confidence: 99%

Combined complementary imaging techniques in morphological analysis of Spongilla lacustris (Linnaeus 1759)

Woźnica

Karczewski

Gwiazda

et al. 2023

Limnology & Ocean Methods

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“…In some groups, they are arranged into rigid (fused) skeletal structures. Siliceous spicules are biocomposites that incorporate organic material in their structure—a special protein complex forming an axial filament situated in the interior of most siliceous spicules (Ehrlich et al, 2022; Görlich et al, 2020; Uriz, 2006; Uriz et al, 2003). Collagen or chitin matrix may be also present inside the silica spicules (Ehrlich et al, 2007, 2017, 2018; Fromont et al, 2019; Pisera et al, 2021).…”

Section: Poriferan Tissue and Skeletonmentioning

confidence: 99%

The terminology of sponge spicules

Łukowiak

Soest

Klautau

et al. 2022

Journal of Morphology

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Sponges (Porifera) are a diverse and globally distributed clade of benthic organisms, with an evolutionary history reaching at least the Ediacaran-Cambrian (541 Ma) boundary interval. Throughout their research history, sponges have been subjects of intense studies in many fields, including paleontology, evolutionary biology, and even bioengineering and pharmacology. The skeletons of sponges are mostly characterized by the presence of mineral elements termed spicules, which structurally support the sponge bodies, though they also minimize the metabolic cost of water exchange and deter predators. The description of the spicules' shape and the skeleton organization represents the fundamental basis of sponge taxonomy and systematics. Here, we provide an illustrated catalogue of sponge spicules, which is based on previous works on sponge spicules, for example, and gathers and updates all terms that are currently used in sponge descriptions. Each spicule type is further illustrated through high quality scanning electron microscope micrographs. It is expected to be a valuable source that will facilitate spicule identification and, in certain cases, also enable sponge classification.

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“…Before we can reach a mechanistic understanding of the dissolution of biogenic silica, further characterization of the BSi behavior in seawater and Si-desaturated solutions rich in ions is required. Likewise, a recent surprising report of actin deeply embedded in the silica of demosponges and hexactinellids (Ehrlich et al, 2022) emphasizes the need of deepening into the atom-level characterization of the complexation of BSi with organic elements, which may significantly determine dissolution patterns. The persisting lack of knowledge in this sense is relevant because the dissolution kinetics of the biogenic silica reservoirs in the water column and the sediments are one of the main controls of the biogeochemical cycling of silicon in the ocean.…”

Section: Dissolution Patterns and Their Causesmentioning

confidence: 99%

On the dissolution of sponge silica: Assessing variability and biogeochemical implications

et al. 2022

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The dissolution of the biogenic silica that constitutes the skeletons of silicifying organisms is an important mechanism for regenerating dissolved silicon in the ocean. The silica skeletons deposited to the seafloor after the organisms die keep dissolving until becoming definitively buried. The low dissolution rate of sponge skeletons compared to that of diatom skeletons favors their burial and makes sponges (Phylum Porifera) to function as important silicon sinks in the oceans. However, it remains poorly understood whether the large variety of siliceous skeletons existing in the Porifera involves similar variability in their dissolution rates, which would affect the general conceptualization of these organisms as silicon sinks. Herein we investigated kinetics of silica dissolution for major types of skeletons in the three siliceous lineages of Porifera, following standardized digestion conditions in 1% sodium carbonate with orbital agitation at 85°C. The results are compared with those of a previous study conducted under identical conditions, which considered diatom silica, sponge silica, and lithogenic silica. Unexpectedly, the silica of homoscleromorph sponges dissolved only a bit slower than that of freshly cultured diatoms and as fast as diatom earth. However, the rest of sponge skeletons were far more resistant, although with some differences: the isolated spicules of hexactinellid sponges dissolved slightly faster than when forming frameworks of fused spicules, being hexactinellid frameworks as resistant to dissolution as the silica of demosponges, irrespective of occurring in the form of isolated spicules or frameworks. The experiments also indicated that the complexation of sponge silica with aluminum and with chitin does not increase its resistance to dissolution. Because the rapidly-dissolving homoscleromorph sponges represent less than 1% of extant sponges, the sponge skeletons are still conceptualized as important silicon sinks due to their comparative resistance to dissolution. Yet, the turnover of silica into dissolved silicon will always be faster in environments dominated by hexactinellids with isolated spicules than in environments dominated by other hexactinellids and/or demosponges. We discuss whether the time required for a given silica type to completely dissolve in 1% sodium carbonate could be a predictor of its preservation ratio in marine sediments.

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Arrested in Glass: Actin within Sophisticated Architectures of Biosilica in Sponges

Cited by 19 publications

References 60 publications

Combined complementary imaging techniques in morphological analysis of Spongilla lacustris (Linnaeus 1759)

Combined complementary imaging techniques in morphological analysis of Spongilla lacustris (Linnaeus 1759)

The terminology of sponge spicules

On the dissolution of sponge silica: Assessing variability and biogeochemical implications

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