Genetic parallels in biomineralization of the calcareous sponge Sycon ciliatum and stony corals

Many animals – from corals to snails to humans – build hard structures such as shells, teeth, and skeletons through a process called biomineralization. In this process, specialized cells deposit minerals like calcium carbonate with the help of dedicated proteins and their genes.

Biomineralization has evolved independently across different animal lineages, often by reusing or modifying existing genes. Among the earliest animals to produce mineralized structures were sponges, many of which form skeletal elements known as spicules. Calcareous sponges, for example, build spicules from calcite, but the underlying genetic and molecular mechanisms remain poorly understood. By contrast, stony corals, which produce aragonite skeletons, have a relatively well-characterized “biomineralization toolkit.” Studying how sponges construct their spicules, therefore, offers a unique opportunity to explore the origins and diversity of biomineralization strategies across animals.

To address this, Voigt et al. investigated the genes and proteins involved in forming calcitic spicules in the calcareous sponge Sycon ciliatum. This species is an excellent model because each spicule is produced by only a few specialized cells, enabling precise analysis of gene expression during biomineralization in a simple system.

Using a combination of transcriptomic, genomic, and proteomic approaches, and a method called RNA in situ hybridization, the team identified 829 genes that were upregulated in spicule-forming areas in the sponge. Among them were 17 calcarins – a newly described group of galaxin-like proteins (which are proteins also found in corals) that were expressed in mineral-secreting cells known as sclerocytes and incorporated into the spicule matrix.

These proteins appear to be unique to calcareous sponges and absent from other sponge lineages. Different spicule types showed distinct patterns of gene activation, suggesting specialized roles. Evidence of gene duplication and neofunctionalization – that is, duplicated genes adopting a new role – was also found. Together, these results suggest molecular parallels between the calcitic spicules of sponges and the aragonitic skeletons of corals, despite their independent evolutionary origins.

These findings deepen our understanding of the evolution and regulation of biomineralization – a process central to marine ecosystems. They may inform future research into how reef-building organisms such as corals and sponges respond to environmental challenges like climate change and ocean acidification. Insights into how organisms control mineral formation could inspire biomimetic materials and sustainable synthesis techniques. Future studies will be needed to explore the functional roles of these genes and their ecological significance.

The evolution of biomineralization allowed animals to produce important mineralized functional structures, such as shells, teeth, and skeletons. For this, they most frequently use calcium carbonate, calcium phosphate, and silicate as mineral components, of which calcium carbonate is taxonomically the most diverse (Knoll, 2003; Murdock and Donoghue, 2011). Animal biominerals are usually composite materials of organic and mineral compounds and exhibit material properties and shapes that differ enormously from their purely mineral counterparts. Their formation requires biological control governed by specific genes and proteins in specialized biomineralization cells and tissues. Those then ensure supply with the necessary inorganic substances into the calcifying space (intracellularly or extracellularly) to enable crystal precipitation and growth, e.g., by pH regulation. They also provide organic components, including secreted, so-called ‘matrix proteins’ that influence the polymorph and shape of the biomineral and subsequently may become embedded in it (Aizenberg et al., 1996; Aizenberg et al., 1994).

The ability to form biominerals evolved several times independently in animal lineages, and early instances of mineralized animal skeletons appeared within a geologically brief span, from the latest Ediacaran to the Middle Cambrian (Murdock and Donoghue, 2011). According to the ‘biomineralization toolkit’ hypothesis, animals of this era had acquired pre-adapted genes and gene-regulatory networks necessary to produce biominerals in a controlled manner that were further refined independently in different lineages (Murdock, 2020). This can be achieved by gene family expansion, in which, after initial gene duplication, diversification by mutation and natural selection leads to the neofunctionalization of a copied gene in the biomineralization process.

Among early branching, non-bilaterian calcifiers, stony corals are best studied, and essential elements of their genetic biomineralization machinery are known that originate from gene duplication and neofunctionalization, such as the SLC4γ bicarbonate transporter (SLC4γ) that is a key component of the coral aragonite skeleton forming machinery (Tinoco et al., 2023; Zoccola et al., 2015). Numerous skeletal matrix proteins have been identified (Drake et al., 2013; Peled et al., 2020; Ramos-Silva et al., 2013). Among those, galaxin and related proteins were the first to be characterized, and at least in some species, comprise the most dominant protein in skeletal matrix extractions (Fukuda et al., 2003; Watanabe et al., 2003). Acidic proteins are another essential component of coral skeletal matrices, presumably influencing the polymorph of the precipitating carbonate (Drake et al., 2013; Laipnik et al., 2020; Mass et al., 2016). However, the genetic mechanisms of the calcium carbonate biomineralization in sponges (class Porifera) are less known. Sponges produce skeletal elements in the form of differently shaped spicules, siliceous in the extant sponge classes Demospongiae, Hexactinellida, and Homoscleromorpha, and calcitic only in the class Calcarea (calcareous sponges). Nonetheless, some demosponges like the polyphyletic ‘sclerosponges’ may form a rigid calcium carbonate basal skeleton in addition to or instead of siliceous spicules (Wörheide, 1998). Essential skeletal matrix proteins occluded in such rigid calcitic carbonate skeletons of sclerosponges have been studied in Astrosclera willeyana (Jackson et al., 2011; Jackson et al., 2007) and Vaceletia sp. (Germer et al., 2015). In contrast to those aragonite-producing sclerosponges, calcareous sponges continuously produce calcitic spicules of different shapes, providing a unique opportunity to observe all stages of the process and study differences in their production. Additionally, their spicule formation is often faster than the production of skeletal elements in other calcifiers. It takes only a few days from initiation to the finished spicule and involves only a few specialized cells called sclerocytes (Ilan et al., 1996; Woodland, 1905). They control biomineralization by their relative movement to each other and by secreting specific proteins, ions, and other substances into the calcification space, a process still little understood at the molecular level. Only a few genes involved in calcification in calcareous sponges are known, including two specific carbonic anhydrases, and two SLC4 bicarbonate transporters, and three acidic proteins, two of which are spicule-type specific (Voigt et al., 2021; Voigt et al., 2017; Voigt et al., 2014). Skeletal matrix proteins have not yet been identified but are of particular interest because they may play a crucial role in spicule morphogenesis (Aizenberg et al., 1995).

In this study, we used genomic data, differential gene expression (DGE) analysis, and RNA in situ hybridization (ISH) experiments, supplemented by a proteomic approach, to identify genes directly involved in the spicule formation in the calcarean model species Sycon ciliatum (subclass Calcaronea), and compare those with another non-bilaterian calcifying clade, the scleractinian (stony) corals, the ecosystem engineers of today’s coral reefs. We found surprising similarities in key components of the biomineralization toolkit between calcareous sponges and corals that shed new light on the evolution of calcium carbonate biomineralization in animals.

Sycon ciliatum is a tube-shaped sponge with a single apical osculum and a sponge wall of radial tubes around the central atrium (Figure 1A). The radial tubes are internally lined with choanoderm, which forms elongated chambers in an angle of approximately 90° to the tube axis. The sponge tissue is supported by a skeleton composed of countless spicules arranged in a specific pattern within the sponge body (Figure 1A). The spicules are formed by sclerocytes located within the mesohyl, the extracellular matrix of the sponge. Connected by septate junctions, they enclose an extracellular space where a spicule grows (Ledger, 1975). Only a small number of sclerocytes participate in forming a single spicule (Figure 1C). Production of each actine (ray) of a spicule involves a pair of sclerocytes (Woodland, 1905): a founder cell, which initiates actine elongation at the tip, and a thickener cell, located alongside the actine. The thickener cell enhances actine strength in some species by precipitating additional calcium carbonate. More spicules are produced in the apical growth zone than in other regions of Sycon’s body (Voigt et al., 2014). In this zone, diactine spicules, one-rayed spicules with two pointed tips, are arranged in a palisade-like manner and continuously grow around the osculum opening. Simultaneously, new triactines, three-rayed spicules resembling a Mercedes star, and four-rayed tetractines form in the atrial skeleton. Large amounts of triactines and distal diactine bundles are also produced within newly developing radial tubes (Figure 1B).

Figure 1

Download asset Open asset

DGE analysis

We performed a DGE analysis comparing gene expression of the apical oscular region to the inner and outer body walls of the more basal body regions in five specimens (Appendix 1—table 1). We observed 1575 differentially expressed genes (log2-fold change ≥2, padj<0.01). Of these genes, 829 were overexpressed in the oscular region, including the known biomineralization genes with documented sclerocyte-specific expression: CA1, CA2, AE-like1, AE-like2, Diactinin, Triactinin, Spiculin (Voigt et al., 2017; Voigt et al., 2014).

To gain further insight into these genes’ potential function, we performed a GO-term enrichment analysis, considering the GO-term annotation of the closest hit in Uniprot against each transcript as a potential annotation for the S. ciliatum genes. The genes overexpressed in the oscular regions were enriched in biological process GO-terms relevant for biomineralization (e.g. with the representative terms GO:0001501 ‘skeletal system development’, GO:0001503: ‘ossification’, GO:0030282 ‘bone mineralization’, Supplementary file 1). Among them were genes similar to Fibrilin-1, Collagen alpha-1 (XXVIII) chain B, Collagen alpha-1 (I) chain, Collagen alpha-1 (XI) chain, V-type proton ATPase subunit a, and to Fibroblast growth factor receptor 2. Additionally, the S. ciliatum-specific growth factor SciTgfBH, with similarity to bone morphogenetic protein 2, and the homeobox protein SciMsx, with similarity to the homeobox protein MSX-2, belong to genes with these enriched GO terms. Other enriched GO terms related to ongoing morphogenesis, cell differentiation, cell signaling, cell migration, and organization of the organic matrix are all indicative of the growth zone that the oscular region represents (Supplementary file 1). Noteworthy among them are genes of the Wnt pathway (SciWntG, I, J, K, L, M, O, U, SciFzdD, and Metalloprotease TIKI homolog).

Fourteen secreted proteins, with significantly higher expression in the oscular region, showed similarity to the coral skeletal organic matrix proteins galaxin and galaxin-like proteins, first described from the coral Galaxea fascicularis (Fukuda et al., 2003; Watanabe et al., 2003). In total, 17 proteins similar to galaxins were identified from the predicted proteins of the S. ciliatum genome using BLASTp. We refer to these as calcarin 1–17 (Cal1–Cal17) to discriminate them from galaxin and galaxin-like proteins of scleractinian corals. The presence of signal peptides indicates that calcarins are secreted. Except for a Reeler domain (Pfam PF02014) in Cal16, calcarins lack recognizable domains. Like galaxins, calcarins contain regions with 10–23 di-cysteine residues, typically separated by 10–15 amino acids. Additionally, a single cysteine occurs approximately at the inter-di-cysteine distance upstream and downstream of the di-cysteine region. Monomer AlphaFold predictions propose that disulfide bridges between these cysteines provide a tertiary structure typical of calcarins and galaxins (Figure 2; Figure 2—figure supplement 1). The di-cysteines form the N-terminal part of a common four-amino acid beta-hairpin with a short, often two-amino acid long turn. The first cysteine of a di-cysteine connects with the second cysteine of the preceding beta-hairpin by a disulfide bridge, linking the beta-hairpins together. This disulfide bridge backbone is continuous in galaxins, whereas the predictions in calcarins may show one or two interruptions.

Figure 2 with 2 supplements see all

Download asset Open asset

Temporal and spatial expression of calcarins

The expression of Cal1 to Cal8 was investigated using chromogenic in situ hybridization (CISH) and hairpin chain reaction fluorescence in situ hybridization (HCR-FISH), confirming their presence in sclerocytes (Figure 3). Additionally, antisense probes were used against the mRNA of Spiculin, an acidic protein specific to all thickener cells, Triactinin, a marker for triactine and tetractine thickener cells, and the sclerocyte-specific carbonic anhydrase SciCA1 (Voigt et al., 2017; Voigt et al., 2014). This approach enabled us to visualize and contextualize calcarin-positive cells (Figure 3—figure supplement 1). The expression patterns of calcarins varied with sclerocyte type and spicule formation stage.

Figure 3 with 3 supplements see all

Download asset Open asset

Cal1 is predominantly observed in the founder cells of triactines and tetractines and only minimal overlap with Cal2 expression (Figure 3A–D). Initially expressed in all six founder cells, expression ceases in the central sclerocytes after they transform into thickener cells. The Cal1 signal persists in the remaining founder cells at the tips of the growing spicules (Figure 3D and E). In the founder cells of the diactines, Cal1 is only expressed transiently, as is evident by the lack of Cal1 signal in most oscular diactine founder cells (Figure 3A and B). Occasionally, we observed co-expression of Spiculin and Cal1 in diactine sclerocytes, presumably during the onset of the conversion of a diactine founder cell to a thickener cell (Figure 3E). At slightly later stages (recognizable by the elongated cell shape), Cal1 is no longer expressed in the thickener cells. At even later stages, Cal1 expression also ceases in the founder cells of the diactines, which instead express Cal2 (Figure 3E, Figure 3—figure supplement 1). The expression of Cal2 and Spiculin can be recognized in two superimposed rings of cells around the osculum, representing the founder cells and the associated thickener cells of the oscular diactines (Figure 3B).

Cal3, Cal7, and Cal8 are produced by all founder cells, regardless of the type of spicule they form (Figure 3F–I and L). During the transformation into thickener cells, the expression of these calcarins ceases and is replaced by the expression of Spiculin. Again, co-expression of some of these calcarins with Spiculin was observed in a few cells, probably in sclerocytes transitioning from founder to thickener cells (Figure 3G). Cal4 is expressed in thickener cells, Cal5 only in thickener cells of triactines, like Spiculin and Triactinin, respectively (Figure 3J). Cal6 expression mirrors that of Cal2, occurring in rounded cells at the distal tip of radial tubes and in a ring of cells around the oscular ring (Figure 3K). In these regions, Spiculin-expressing cells are spatially associated. In regions without diactines, like the atrial cavity, no Cal6 expression occurs, even if Spiculin expression indicates ongoing production of triactines and tetractines (Figure 3—figure supplement 2). Like Cal2, Cal6 must be expressed by later-stage diactine founder cells, which appear more spherical than elongated. At the end of radial tubes, Cal2 and Cal6 positive founder cells are in contact with choanocytes (Figure 3—figure supplement 2A). In summary, calcarin expression in sclerocytes varies across spicule formation stages and between sclerocytes of different spicule types (Figure 4), adding further complexity to the spatiotemporal expression of biomineralization genes that was reported before (Voigt et al., 2017). Notably, in young coral polyps, normalized and scaled expression data of the raw cell counts of 980 calicoblastic cells indicate nonoverlapping expression of two galaxin-like proteins, an uncharacterized skeletal matrix protein and a skeletal-aspartic acid-rich protein (Appendix 2—figure 1), suggesting spatiotemporal expression changes of skeletal matrix proteins also occur in calicoblastic cells of corals.

Figure 4

Download asset Open asset

Calcarins and other proteins are embedded in the spicule matrix

We extracted spicules from the tissue using sodium hypochlorite to examine the proteins incorporated in the biomineral. The spicules were then washed with water and dissolved in acetic acid. Mass spectrometry was employed to analyze the acid-insoluble proteins, while the acid-soluble ones were too diluted for adequate examination. With the obtained spectra, we identified 35 proteins (1.0% FDR protein threshold, with at least two peptides per protein, Supplementary file 2). Fifteen of these proteins are encoded by overexpressed transcripts in the oscular region (Figure 5A; Supplementary file 2). We consider these proteins to be specialized biomineralization proteins. Several calcarins expressed in founder cells (Cal1, Cal2, Cal3, Cal7, Cal8) were most prominent. Additional calcarins of the skeletal matrix were Cal9, Cal11, and Cal10, although the latter was only supported by one peptide.

Figure 5

Download asset Open asset

In addition, we found three secreted proteins without any domain or other prominent features other than a signal peptide, which we refer to as skeletal matrix proteins 1–3 (SMP 1–3). Other spicule matrix proteins contain recognizable domains. Two proteins, similar to cysteine-rich secretory protein LCCL domain-containing 2-like (CAH0893205) and peptidase inhibitor 15-like protein (CAH0891878), both belong to the CAP superfamily. Further, we detected a fibronectin III-domain-containing protein (CAH0869470), a subtilisin-like protease (CAH0797261), and an EGF-like domain-containing protein (CAH0821874). Both the LCCL domain-containing 2-like protein and the fibronectin III-domain-containing protein are acidic with isoelectric points of 4.34 and 4.75, respectively. Thickener cell-specific proteins, such as Cal4, Cal5, or the Asx-rich proteins Triactinin and Spiculin, were not observed in the spicule matrix.

When comparing the 15 spicule matrix proteins of Sycon to the skeletal matrix proteins of a Vaceletia sp. (Germer et al., 2015), a demosponge with a calcium carbonate (aragonite) basal skeleton, their similarity is limited to subtilisin-like proteases found in both proteomes. Additional similarity can be seen only in eight additional proteins of presumably intracellular origin (annotated as or containing domains of Histones, Actin, Tubulin, Elongation factor 1a, mitochondrial ATP synthase alpha, Supplementary file 3), which were not overexpressed in the oscular region of S. ciliatum. These proteins may represent ubiquitous extracellular matrix components or, particularly in the case of proteins with intracellular origins, could result from contamination by residual cellular material or their incorporation into the forming biomineral, as suggested before (Ramos-Silva et al., 2013; Germer et al., 2015), and we do not consider them to have specific function in biomineralization.

Sequential order and expression of biomineralization genes

In the S. ciliatum genome, the 17 calcarins occur on chromosomes 1, 2, 4, 7, and 13. On chromosome 2, Cal12, Cal4, Cal6, and Cal2 are positioned sequentially (Figure 6 and Supplementary file 7). Cal4, Cal6, and Cal2 belong to a single orthogroup, indicating their homology. Cal4 is expressed in thickener cells, while Cal2 and Cal6 have identical expression patterns, suggesting they are produced by diactine founder cells during the late diactine formation stage (see above). Cal12 has low expression levels, and we did not locate its expression. The founder cell-specific carbonic anhydrase gene CA2 is situated on the reverse strand of chromosome 4, flanked by CA8 and CA3 on the forward strand. Upstream on the same chromosome, other membrane-bound carbonic anhydrases (Voigt et al., 2021) are present, including CA4, CA5, CA6, and CA7.

Figure 6

Download asset Open asset

In the coral A. millepora, Galaxin1 and Galaxin2 are located subsequently on the genome, making a past gene duplication likely as well. The galaxin-like proteins 1 and 3 also occur in subsequent pairs or triplets. The genes for galaxin-like 2, 1, and 5, as well as galaxin-like 3 and 4, are separated by a maximum of two short predicted genes (Figure 6).

Sequencing data have been deposited in ENA under BioProject accession code PRJEB78728. Mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository (Perez-Riverol et al., 2019) under accession code PXD060105. Scripts and input files for the RNA-Seq, GO-Term, and WGCNA analyses are available in a GitHub repository (https://github.com/PalMuc/CalcBiomin, copy archived at Voigt, 2025) and have been archived within a Zenodo repository https://doi.org/10.5281/zenodo.16786067. De novo gene predictions, detailed outputs from Alpha-Fold and the OrthoFinder-Analysis are provided along with a scaffold file for the proteins identified from the spicule matrix and can be accessed via Zenodo (https://doi.org/10.5281/zenodo.14755899). All data generated or analysed during this study are included in the manuscript and supporting files (Appendix 1 - table 1, Appendix 1 - table 2, Appendix 1 - table 3).

1. 1. Voigt et al.

   (2025) European Nucleotide Archive

   ID PRJEB78728. Calcareous sponge biomineralization.

   https://www.ebi.ac.uk/ena/browser/view/PRJEB78728
2. 1. Voigt O

   (2025) Zenodo

   Supplementary data for "Genetic parallels in biomineralization of the calcareous sponge Sycon ciliatum and stony corals".

   https://doi.org/10.5281/zenodo.14755899
3. 1. Fröhlich T

   (2025) ProteomeXchange

   ID PXD060105. Identification and analysis of organic matrix proteins from Sycon ciliatum spicules.

   https://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD060105
4. 1. Voigt O

   (2025) Zenodo

   PalMuc/CalcBiomin: Updated README, minor bug fixes.

   https://doi.org/10.5281/zenodo.16786067

1. 1. Soubigou et al.

   (2020) European Nucleotide Archive

   ID PRJNA628727. Regeneration in sponge Sycon ciliatum partly mimics postlarval development.

   https://www.ebi.ac.uk/ena/browser/view/PRJNA628727

1. 1. Aizenberg J
   2. Albeck S
   3. Weiner S
   4. Addadi L

   (1994) Crystal-protein interactions studied by overgrowth of calcite on biogenic skeletal elements

   Journal of Crystal Growth 142:156–164.

   https://doi.org/10.1016/0022-0248(94)90283-6

   • Google Scholar
2. 1. Aizenberg J
   2. Hanson J
   3. Ilan M
   4. Leiserowitz L
   5. Koetzle TF
   6. Addadi L
   7. Weiner S

   (1995) Morphogenesis of calcitic sponge spicules: A role for specialized proteins interacting with growing crystals

   FASEB Journal 9:262–268.

   https://doi.org/10.1096/fasebj.9.2.7781928

   • PubMed
   • Google Scholar
3. 1. Aizenberg J
   2. Ilan M
   3. Weiner S
   4. Addadi L

   (1996) Intracrystalline macromolecules are involved in the morphogenesis of calcitic sponge spicules

   Connective Tissue Research 34:255–261.

   https://doi.org/10.3109/03008209609005269

   • PubMed
   • Google Scholar
4. 1. Aizenberg J
   2. Weiner S
   3. Addadi L

   (2003) Coexistence of amorphous and crystalline calcium carbonate in skeletal tissues

   Connective Tissue Research 44:20–25.

   https://doi.org/10.1080/03008200390152034

   • PubMed
   • Google Scholar
5. Software

   1. Alexa A
   2. Rahnenfuhrer J

   (2023) Enrichment analysis for gene ontology, version version 2.56.0

   R Package.

   https://bioconductor.org/packages/topGO
6. 1. Bateman A
   2. Martin M-J
   3. Orchard S
   4. Magrane M
   5. Agivetova R
   6. Ahmad S
   7. Alpi E
   8. Bowler-Barnett EH
   9. Britto R
   10. Bursteinas B
   11. Bye-A-Jee H
   12. Coetzee R
   13. Cukura A
   14. Da Silva A
   15. Denny P
   16. Dogan T
   17. Ebenezer T
   18. Fan J
   19. Castro LG
   20. Garmiri P
   21. Georghiou G
   22. Gonzales L
   23. Hatton-Ellis E
   24. Hussein A
   25. Ignatchenko A
   26. Insana G
   27. Ishtiaq R
   28. Jokinen P
   29. Joshi V
   30. Jyothi D
   31. Lock A
   32. Lopez R
   33. Luciani A
   34. Luo J
   35. Lussi Y
   36. MacDougall A
   37. Madeira F
   38. Mahmoudy M
   39. Menchi M
   40. Mishra A
   41. Moulang K
   42. Nightingale A
   43. Oliveira CS
   44. Pundir S
   45. Qi G
   46. Raj S
   47. Rice D
   48. Lopez MR
   49. Saidi R
   50. Sampson J
   51. Sawford T
   52. Speretta E
   53. Turner E
   54. Tyagi N
   55. Vasudev P
   56. Volynkin V
   57. Warner K
   58. Watkins X
   59. Zaru R
   60. Zellner H
   61. Bridge A
   62. Poux S
   63. Redaschi N
   64. Aimo L
   65. Argoud-Puy G
   66. Auchincloss A
   67. Axelsen K
   68. Bansal P
   69. Baratin D
   70. Blatter M-C
   71. Bolleman J
   72. Boutet E
   73. Breuza L
   74. Casals-Casas C
   75. de Castro E
   76. Echioukh KC
   77. Coudert E
   78. Cuche B
   79. Doche M
   80. Dornevil D
   81. Estreicher A
   82. Famiglietti ML
   83. Feuermann M
   84. Gasteiger E
   85. Gehant S
   86. Gerritsen V
   87. Gos A
   88. Gruaz-Gumowski N
   89. Hinz U
   90. Hulo C
   91. Hyka-Nouspikel N
   92. Jungo F
   93. Keller G
   94. Kerhornou A
   95. Lara V
   96. Le Mercier P
   97. Lieberherr D
   98. Lombardot T
   99. Martin X
   100. Masson P
   101. Morgat A
   102. Neto TB
   103. Paesano S
   104. Pedruzzi I
   105. Pilbout S
   106. Pourcel L
   107. Pozzato M
   108. Pruess M
   109. Rivoire C
   110. Sigrist C
   111. Sonesson K
   112. Stutz A
   113. Sundaram S
   114. Tognolli M
   115. Verbregue L
   116. Wu CH
   117. Arighi CN
   118. Arminski L
   119. Chen C
   120. Chen Y
   121. Garavelli JS
   122. Huang H
   123. Laiho K
   124. McGarvey P
   125. Natale DA
   126. Ross K
   127. Vinayaka CR
   128. Wang Q
   129. Wang Y
   130. Yeh L-S
   131. Zhang J
   132. Ruch P
   133. Teodoro D
   134. The UniProt Consortium

   (2021) UniProt: the universal protein knowledgebase in 2021

   Nucleic Acids Research 49:D480–D489.

   https://doi.org/10.1093/nar/gkaa1100

   • Google Scholar
7. 1. Bertucci A
   2. Moya A
   3. Tambutté S
   4. Allemand D
   5. Supuran CT
   6. Zoccola D

   (2013) Carbonic anhydrases in anthozoan corals-A review

   Bioorganic & Medicinal Chemistry 21:1437–1450.

   https://doi.org/10.1016/j.bmc.2012.10.024

   • PubMed
   • Google Scholar
8. Preprint

   1. Caglar C
   2. Ereskovsky A
   3. Laplante M
   4. Tokina D
   5. Leininger S
   6. Borisenko I
   7. Aisbett G
   8. Pan D
   9. Adamski M
   10. Adamska M

   (2021) Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

   bioRxiv.

   https://doi.org/10.1101/2021.07.22.453456

   • Google Scholar
9. 1. Camacho C
   2. Coulouris G
   3. Avagyan V
   4. Ma N
   5. Papadopoulos J
   6. Bealer K
   7. Madden TL

   (2009) BLAST+: Architecture and applications

   BMC Bioinformatics 10:421.

   https://doi.org/10.1186/1471-2105-10-421

   • PubMed
   • Google Scholar
10. 1. Conci N
    2. Lehmann M
    3. Vargas S
    4. Wörheide G

    (2020) Comparative proteomics of octocoral and scleractinian skeletomes and the evolution of coral calcification

    Genome Biology and Evolution 12:1623–1635.

    https://doi.org/10.1093/gbe/evaa162

    • PubMed
    • Google Scholar
11. 1. Creasy DM
    2. Perkins DN
    3. Pappin DJC
    4. Cottrell JS

    (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data

    Electrophoresis 1:35513022.

    https://doi.org/10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2

    • Google Scholar
12. 1. Drake JL
    2. Mass T
    3. Haramaty L
    4. Zelzion E
    5. Bhattacharya D
    6. Falkowski PG

    (2013) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata

    PNAS 110:3788–3793.

    https://doi.org/10.1073/pnas.1301419110

    • PubMed
    • Google Scholar
13. 1. Edgar RC

    (2004) MUSCLE: A multiple sequence alignment method with reduced time and space complexity

    BMC Bioinformatics 5:113.

    https://doi.org/10.1186/1471-2105-5-113

    • PubMed
    • Google Scholar
14. Software

    1. Elek A

    (2025) Stylophora_single_cell_atlas, version 09960d4

    GitHub.

    https://github.com/sebepedroslab/Stylophora_single_cell_atlas
15. 1. Emms DM
    2. Kelly S

    (2019) OrthoFinder: Phylogenetic orthology inference for comparative genomics

    Genome Biology 20:238.

    https://doi.org/10.1186/s13059-019-1832-y

    • PubMed
    • Google Scholar
16. 1. Fortunato S
    2. Adamski M
    3. Bergum B
    4. Guder C
    5. Jordal S
    6. Leininger S
    7. Zwafink C
    8. Rapp HT
    9. Adamska M

    (2012) Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: Multiple genes with unique expression patterns

    EvoDevo 3:14.

    https://doi.org/10.1186/2041-9139-3-14

    • PubMed
    • Google Scholar
17. 1. Fortunato SAV
    2. Adamski M
    3. Ramos OM
    4. Leininger S
    5. Liu J
    6. Ferrier DEK
    7. Adamska M

    (2014) Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes

    Nature 514:620–623.

    https://doi.org/10.1038/nature13881

    • PubMed
    • Google Scholar
18. Preprint

    1. Francis WR
    2. Eitel M
    3. Vargas S
    4. Adamski M
    5. Haddock SHD
    6. Krebs S
    7. Blum H
    8. Erpenbeck D
    9. Wörheide G

    (2017) The genome of the contractile demosponge Tethya wilhelma and the evolution of metazoan neural signalling pathways

    bioRxiv.

    https://doi.org/10.1101/120998

    • Google Scholar
19. Software

    1. Francis WR

    (2023) Aphrocallistes_vastus_genome, version 2ba7512

    Github.

    https://github.com/PalMuc/Aphrocallistes_vastus_genome/
20. 1. Francis WR
    2. Eitel M
    3. Vargas S
    4. Garcia-Escudero CA
    5. Conci N
    6. Deister F
    7. Mah JL
    8. Guiglielmoni N
    9. Krebs S
    10. Blum H
    11. Leys SP
    12. Wörheide G

    (2023) The genome of the reef-building glass sponge Aphrocallistes vastus provides insights into silica biomineralization

    Royal Society Open Science 10:230423.

    https://doi.org/10.1098/rsos.230423

    • PubMed
    • Google Scholar
21. 1. Fukuda I
    2. Ooki S
    3. Fujita T
    4. Murayama E
    5. Nagasawa H
    6. Isa Y
    7. Watanabe T

    (2003) Molecular cloning of a cDNA encoding a soluble protein in the coral exoskeleton

    Biochemical and Biophysical Research Communications 304:11–17.

    https://doi.org/10.1016/s0006-291x(03)00527-8

    • PubMed
    • Google Scholar
22. 1. Germer J
    2. Mann K
    3. Wörheide G
    4. Jackson DJ

    (2015) The skeleton forming proteome of an early branching metazoan: A molecular survey of the biomineralization components employed by the coralline sponge Vaceletia sp

    PLOS ONE 10:e0140100.

    https://doi.org/10.1371/journal.pone.0140100

    • PubMed
    • Google Scholar
23. 1. Hao Y
    2. Stuart T
    3. Kowalski MH
    4. Choudhary S
    5. Hoffman P
    6. Hartman A
    7. Srivastava A
    8. Molla G
    9. Madad S
    10. Fernandez-Granda C
    11. Satija R

    (2024) Dictionary learning for integrative, multimodal and scalable single-cell analysis

    Nature Biotechnology 42:293–304.

    https://doi.org/10.1038/s41587-023-01767-y

    • PubMed
    • Google Scholar
24. 1. Ilan M
    2. Aizenberg J
    3. Gilor O

    (1996) Dynamics and growth patterns of calcareous sponge spicules

    Proceedings of the Royal Society of London. Series B 263:133–139.

    https://doi.org/10.1098/rspb.1996.0021

    • Google Scholar
25. 1. Jackson DJ
    2. Macis L
    3. Reitner J
    4. Degnan BM
    5. Wörheide G

    (2007) Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis

    Science 316:1893–1895.

    https://doi.org/10.1126/science.1141560

    • PubMed
    • Google Scholar
26. 1. Jackson DJ
    2. Macis L
    3. Reitner J
    4. Wörheide G

    (2011) A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy

    BMC Evolutionary Biology 11:238.

    https://doi.org/10.1186/1471-2148-11-238

    • PubMed
    • Google Scholar
27. 1. Kearse M
    2. Moir R
    3. Wilson A
    4. Stones-Havas S
    5. Cheung M
    6. Sturrock S
    7. Buxton S
    8. Cooper A
    9. Markowitz S
    10. Duran C
    11. Thierer T
    12. Ashton B
    13. Meintjes P
    14. Drummond A

    (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data

    Bioinformatics 28:1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    • PubMed
    • Google Scholar
28. 1. Kenny NJ
    2. Francis WR
    3. Rivera-Vicéns RE
    4. Juravel K
    5. de Mendoza A
    6. Díez-Vives C
    7. Lister R
    8. Bezares-Calderón LA
    9. Grombacher L
    10. Roller M
    11. Barlow LD
    12. Camilli S
    13. Ryan JF
    14. Wörheide G
    15. Hill AL
    16. Riesgo A
    17. Leys SP

    (2020) Tracing animal genomic evolution with the chromosomal-level assembly of the freshwater sponge Ephydatia muelleri

    Nature Communications 11:3676.

    https://doi.org/10.1038/s41467-020-17397-w

    • PubMed
    • Google Scholar
29. 1. Kim D
    2. Paggi JM
    3. Park C
    4. Bennett C
    5. Salzberg SL

    (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype

    Nature Biotechnology 37:907–915.

    https://doi.org/10.1038/s41587-019-0201-4

    • PubMed
    • Google Scholar
30. 1. Knoll AH

    (2003) Biomineralization and Evolutionary History

    Reviews in Mineralogy and Geochemistry 54:329–356.

    https://doi.org/10.2113/0540329

    • Google Scholar
31. 1. Laipnik R
    2. Bissi V
    3. Sun C-Y
    4. Falini G
    5. Gilbert PUPA
    6. Mass T

    (2020) Coral acid rich protein selects vaterite polymorph in vitro

    Journal of Structural Biology 209:107431.

    https://doi.org/10.1016/j.jsb.2019.107431

    • Google Scholar
32. 1. Langfelder P
    2. Horvath S

    (2008) WGCNA: An R package for weighted correlation network analysis

    BMC Bioinformatics 9:559.

    https://doi.org/10.1186/1471-2105-9-559

    • PubMed
    • Google Scholar
33. 1. Langfelder P
    2. Horvath S

    (2012) Fast R functions for robust correlations and hierarchical clustering

    Journal of Statistical Software 46:i11.

    https://doi.org/10.18637/jss.v046.i11

    • PubMed
    • Google Scholar
34. 1. Ledger PW

    (1975) Septate junctions in the calcareous sponge Sycon ciliatum

    Tissue & Cell 7:13–18.

    https://doi.org/10.1016/s0040-8166(75)80004-8

    • PubMed
    • Google Scholar
35. 1. Le Roy N
    2. Ganot P
    3. Aranda M
    4. Allemand D
    5. Tambutté S

    (2021) The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals

    BMC Ecology and Evolution 21:1.

    https://doi.org/10.1186/s12862-020-01734-0

    • PubMed
    • Google Scholar
36. 1. Levy S
    2. Elek A
    3. Grau-Bové X
    4. Menéndez-Bravo S
    5. Iglesias M
    6. Tanay A
    7. Mass T
    8. Sebé-Pedrós A

    (2021) A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity

    Cell 184:2973–2987.

    https://doi.org/10.1016/j.cell.2021.04.005

    • PubMed
    • Google Scholar
37. 1. Love MI
    2. Huber W
    3. Anders S

    (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

    Genome Biology 15:550.

    https://doi.org/10.1186/s13059-014-0550-8

    • PubMed
    • Google Scholar
38. 1. Manni M
    2. Berkeley MR
    3. Seppey M
    4. Simão FA
    5. Zdobnov EM

    (2021) BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes

    Molecular Biology and Evolution 38:4647–4654.

    https://doi.org/10.1093/molbev/msab199

    • PubMed
    • Google Scholar
39. 1. Mass T
    2. Putnam HM
    3. Drake JL
    4. Zelzion E
    5. Gates RD
    6. Bhattacharya D
    7. Falkowski PG

    (2016) Temporal and spatial expression patterns of biomineralization proteins during early development in the stony coral Pocillopora damicornis

    Proceedings of the Royal Society B 283:20160322.

    https://doi.org/10.1098/rspb.2016.0322

    • Google Scholar
40. 1. Murdock DJE
    2. Donoghue PCJ

    (2011) Evolutionary origins of animal skeletal biomineralization

    Cells Tissues Organs 194:98–102.

    https://doi.org/10.1159/000324245

    • Google Scholar
41. 1. Murdock DJE

    (2020) The ‘biomineralization toolkit’ and the origin of animal skeletons

    Biological Reviews 95:1372–1392.

    https://doi.org/10.1111/brv.12614

    • Google Scholar
42. 1. Patro R
    2. Duggal G
    3. Love MI
    4. Irizarry RA
    5. Kingsford C

    (2017) Salmon provides fast and bias-aware quantification of transcript expression

    Nature Methods 14:417–419.

    https://doi.org/10.1038/nmeth.4197

    • PubMed
    • Google Scholar
43. 1. Peled Y
    2. Drake JL
    3. Malik A
    4. Almuly R
    5. Lalzar M
    6. Morgenstern D
    7. Mass T

    (2020) Optimization of skeletal protein preparation for LC-MS/MS sequencing yields additional coral skeletal proteins in Stylophora pistillata

    BMC Materials 2:8.

    https://doi.org/10.1186/s42833-020-00014-x

    • PubMed
    • Google Scholar
44. 1. Perez-Riverol Y
    2. Csordas A
    3. Bai J
    4. Bernal-Llinares M
    5. Hewapathirana S
    6. Kundu DJ
    7. Inuganti A
    8. Griss J
    9. Mayer G
    10. Eisenacher M
    11. Pérez E
    12. Uszkoreit J
    13. Pfeuffer J
    14. Sachsenberg T
    15. Yilmaz S
    16. Tiwary S
    17. Cox J
    18. Audain E
    19. Walzer M
    20. Jarnuczak AF
    21. Ternent T
    22. Brazma A
    23. Vizcaíno JA

    (2019) The PRIDE database and related tools and resources in 2019: Improving support for quantification data

    Nucleic Acids Research 47:D442–D450.

    https://doi.org/10.1093/nar/gky1106

    • PubMed
    • Google Scholar
45. 1. Ramos-Silva P
    2. Kaandorp J
    3. Huisman L
    4. Marie B
    5. Zanella-Cléon I
    6. Guichard N
    7. Miller DJ
    8. Marin F

    (2013) The skeletal proteome of the coral Acropora millepora: The evolution of calcification by co-option and domain shuffling

    Molecular Biology and Evolution 30:2099–2112.

    https://doi.org/10.1093/molbev/mst109

    • PubMed
    • Google Scholar
46. 1. Reyes-Bermudez A
    2. Lin Z
    3. Hayward DC
    4. Miller DJ
    5. Ball EE

    (2009) Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora

    BMC Evolutionary Biology 9:178.

    https://doi.org/10.1186/1471-2148-9-178

    • PubMed
    • Google Scholar
47. 1. Rivera-Vicéns RE
    2. Garcia-Escudero CA
    3. Conci N
    4. Eitel M
    5. Wörheide G

    (2022) TransPi-a comprehensive TRanscriptome ANalysiS PIpeline for de novo transcriptome assembly

    Molecular Ecology Resources 22:2070–2086.

    https://doi.org/10.1111/1755-0998.13593

    • PubMed
    • Google Scholar
48. 1. Sánchez-Duffhues G
    2. Hiepen C
    3. Knaus P
    4. Ten Dijke P

    (2015) Bone morphogenetic protein signaling in bone homeostasis

    Bone 80:43–59.

    https://doi.org/10.1016/j.bone.2015.05.025

    • PubMed
    • Google Scholar
49. 1. Sehnal D
    2. Bittrich S
    3. Deshpande M
    4. Svobodová R
    5. Berka K
    6. Bazgier V
    7. Velankar S
    8. Burley SK
    9. Koča J
    10. Rose AS

    (2021) Mol* Viewer: modern web app for 3D visualization and analysis of large biomolecular structures

    Nucleic Acids Research 49:W431–W437.

    https://doi.org/10.1093/nar/gkab314

    • PubMed
    • Google Scholar
50. 1. Shimizu K
    2. Nishi M
    3. Sakate Y
    4. Kawanami H
    5. Bito T
    6. Arima J
    7. Leria L
    8. Maldonado M

    (2024) Silica-associated proteins from hexactinellid sponges support an alternative evolutionary scenario for biomineralization in Porifera

    Nature Communications 15:181.

    https://doi.org/10.1038/s41467-023-44226-7

    • PubMed
    • Google Scholar
51. 1. Soubigou A
    2. Ross EG
    3. Touhami Y
    4. Chrismas N
    5. Modepalli V

    (2020) Regeneration in the sponge Sycon ciliatum partly mimics postlarval development

    Development 147:dev193714.

    https://doi.org/10.1242/dev.193714

    • PubMed
    • Google Scholar
52. 1. Supek F
    2. Bošnjak M
    3. Škunca N
    4. Šmuc T

    (2011) REVIGO summarizes and visualizes long lists of gene ontology terms

    PLOS ONE 6:e21800.

    https://doi.org/10.1371/journal.pone.0021800

    • PubMed
    • Google Scholar
53. 1. Takeuchi T
    2. Yamada L
    3. Shinzato C
    4. Sawada H
    5. Satoh N

    (2016) Stepwise evolution of coral biomineralization revealed with genome-wide proteomics and transcriptomics

    PLOS ONE 11:e0156424.

    https://doi.org/10.1371/journal.pone.0156424

    • PubMed
    • Google Scholar
54. 1. Tinoco AI
    2. Mitchison-Field LMY
    3. Bradford J
    4. Renicke C
    5. Perrin D
    6. Bay LK
    7. Pringle JR
    8. Cleves PA

    (2023) Role of the bicarbonate transporter SLC4γ in stony-coral skeleton formation and evolution

    PNAS 120:e2216144120.

    https://doi.org/10.1073/pnas.2216144120

    • Google Scholar
55. 1. Voigt O
    2. Adamski M
    3. Sluzek K
    4. Adamska M

    (2014) Calcareous sponge genomes reveal complex evolution of α-carbonic anhydrases and two key biomineralization enzymes

    BMC Evolutionary Biology 14:230.

    https://doi.org/10.1186/s12862-014-0230-z

    • PubMed
    • Google Scholar
56. 1. Voigt O
    2. Adamska M
    3. Adamski M
    4. Kittelmann A
    5. Wencker L
    6. Wörheide G

    (2017) Spicule formation in calcareous sponges: Coordinated expression of biomineralization genes and spicule-type specific genes

    Scientific Reports 7:45658.

    https://doi.org/10.1038/srep45658

    • PubMed
    • Google Scholar
57. 1. Voigt O
    2. Fradusco B
    3. Gut C
    4. Kevrekidis C
    5. Vargas S
    6. Wörheide G

    (2021) Carbonic anhydrases: An ancient tool in calcareous sponge biomineralization

    Frontiers in Genetics 12:624533.

    https://doi.org/10.3389/fgene.2021.624533

    • PubMed
    • Google Scholar
58. Software

    1. Voigt O

    (2025) CalcBiomin, version swh:1:rev:f0934b85ce6e0b42f2df4826d363f807ff5aa876

    Software Heritage.

    https://archive.softwareheritage.org/swh:1:dir:886f0f9d4525ffaac0750f2d35164e63d3a462e6;origin=https://github.com/PalMuc/CalcBiomin;visit=swh:1:snp:6a784fb8ed7e4d0f808774159d735590c519f8da;anchor=swh:1:rev:f0934b85ce6e0b42f2df4826d363f807ff5aa876
59. 1. Watanabe T
    2. Fukuda I
    3. China K
    4. Isa Y

    (2003) Molecular analyses of protein components of the organic matrix in the exoskeleton of two scleractinian coral species

    Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 136:767–774.

    https://doi.org/10.1016/s1096-4959(03)00177-5

    • PubMed
    • Google Scholar
60. 1. Wendt C
    2. de Medeiros FC
    3. Gonçalves RP
    4. Nudelman F
    5. Klautau M
    6. Farina M
    7. Rossi AL

    (2025) Calcium carbonate deposition in the spicules of the sponge Heteropia glomerosa (Porifera, Calcarea)

    Journal of Structural Biology 217:108210.

    https://doi.org/10.1016/j.jsb.2025.108210

    • PubMed
    • Google Scholar
61. 1. Woodland W

    (1905) Memoirs: Studies in spicule formation: I.--The development and structure of the spicules in Sycons: with remarks on the conformation, modes of disposition and evolution of spicules in calcareous sponges generally

    The Quarterly Journal of Microscopical Science 49:231–282.

    https://doi.org/10.1242/jcs.s2-49.194.231

    • Google Scholar
62. 1. Wörheide G

    (1998) The reef cave dwelling ultraconservative coralline demosponge Astrosclera willeyana Lister 1900 from the Indo-Pacific

    Facies 38:1–88.

    https://doi.org/10.1007/BF02537358

    • Google Scholar
63. 1. Zhong Z
    2. Ethen NJ
    3. Williams BO

    (2014) WNT signaling in bone development and homeostasis

    Wiley Interdisciplinary Reviews. Developmental Biology 3:489–500.

    https://doi.org/10.1002/wdev.159

    • PubMed
    • Google Scholar
64. 1. Zoccola D
    2. Ganot P
    3. Bertucci A
    4. Caminiti-Segonds N
    5. Techer N
    6. Voolstra CR
    7. Aranda M
    8. Tambutté E
    9. Allemand D
    10. Casey JR
    11. Tambutté S

    (2015) Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification

    Scientific Reports 5:09983.

    https://doi.org/10.1038/srep09983

    • Google Scholar

Author details

1. Oliver Voigt

   Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig Maximilians-Universität München, Munich, Germany

   Contribution

   Conceptualization, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing – original draft, Project administration, Writing – review and editing, Obtained funding, designed the research approach, planned the experimental work, performed in situ hybridization, analyzed RNA-seq data, submitted sequence data to ENA, prepared figures, wrote the initial draft, and contributed to manuscript editing and revision

   For correspondence

   oliver.voigt@lmu.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8708-0872

2. Magdalena V Wilde

   1. Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig Maximilians-Universität München, Munich, Germany
   2. Gene Center—Laboratory for Functional Genome Analysis, Ludwig-Maximilians-Universität München, Munich, Germany

   Contribution

   Data curation, Formal analysis, Investigation, Methodology, Data generation and analysis (proteome)

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1997-8768

3. Thomas Fröhlich

   Gene Center—Laboratory for Functional Genome Analysis, Ludwig-Maximilians-Universität München, Munich, Germany

   Contribution

   Resources, Formal analysis, Investigation, Writing – review and editing, Data generation and analysis (proteome)

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4709-3211

4. Benedetta Fradusco

   Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig Maximilians-Universität München, Munich, Germany

   Contribution

   Investigation, Data generation: RNA extraction, library preparation

   Competing interests

   No competing interests declared

5. Sergio Vargas

   Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig Maximilians-Universität München, Munich, Germany

   Contribution

   Investigation, Methodology, Support in data analysis, providing predicted proteins of transcriptomes

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8704-1339

6. Gert Wörheide

   1. Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig Maximilians-Universität München, Munich, Germany
   2. GeoBio-Center, Ludwig-Maximilians-Universität München, Munich, Germany

   Contribution

   Conceptualization, Resources, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6380-7421

• 2,763

  views

• 60

  downloads

• 0

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.