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Gert Wörheide

Publications and source records attributed to Gert Wörheide.

8 recordsLinked to original sources

A rapidly evolving secretome builds and patterns a sea shell.

BACKGROUND: Instructions to fabricate mineralized structures with distinct nanoscale architectures, such as seashells and coral and vertebrate skeletons, are encoded in the genomes of a wide variety of animals. In mollusks, the mantle is responsible for the extracellular production of the shell, directing the ordered biomineralization of CaCO3 and the deposition of architectural and color patterns. The evolutionary origins of the ability to synthesize calcified structures across various metazoan taxa remain obscure, with only a small number of protein families identified from molluskan shells. The recent sequencing of a wide range of metazoan genomes coupled with the analysis of gene expression in non-model animals has allowed us to investigate the evolution and process of biomineralization in gastropod mollusks. RESULTS: Here we show that over 25% of the genes expressed in the mantle of the vetigastropod Haliotis asinina encode secreted proteins, indicating that hundreds of proteins are likely to be contributing to shell fabrication and patterning. Almost 85% of the secretome encodes novel proteins; remarkably, only 19% of these have identifiable homologues in the full genome of the patellogastropod Lottia scutum. The spatial expression profiles of mantle genes that belong to the secretome is restricted to discrete mantle zones, with each zone responsible for the fabrication of one of the structural layers of the shell. Patterned expression of a subset of genes along the length of the mantle is indicative of roles in shell ornamentation. For example, Has-sometsuke maps precisely to pigmentation patterns in the shell, providing the first case of a gene product to be involved in molluskan shell pigmentation. We also describe the expression of two novel genes involved in nacre (mother of pearl) deposition. CONCLUSION: The unexpected complexity and evolvability of this secretome and the modular design of the molluskan mantle enables diversification of shell strength and design, and as such must contribute to the variety of adaptive architectures and colors found in mollusk shells. The composition of this novel mantle-specific secretome suggests that there are significant molecular differences in the ways in which gastropods synthesize their shells.

Animal Structures↗

The fatty acids of calcareous sponges (Calcarea, Porifera).

Twenty-nine specimens of calcareous sponges (Class Calcarea, Phylum Porifera), covering thirteen representative species of the families Soleneiscidae, Leucaltidae, Levinellidae, Leucettidae, Clathrinidae, Sycettidae, Grantiidae, Jenkinidae, and Heteropiidae were analysed for their fatty acids. The fatty acids of Calcarea generally comprise saturated and monounsaturated linear (n-), and terminally methylated (iso-, anteiso-) C(14)-C(20) homologues. Furthermore, polyunsaturated C(22) fatty acids and the isoprenoic 4,8,12-trimethyltridecanoic acid were found. The most prominent compounds are n-C(16), iso-C(17), iso-C(18), n-C(18), n-C(20). In addition, a high abundance of the exotic 16-methyloctadecanoic acid (anteiso-C(19)) appears to be a characteristic trait of Calcarea. Long-chain 'demospongic acids', typically found in Demospongiae and Hexactinellida, are absent in Calcarea. The completely different strategy of calcarean fatty acid synthesis supports their phylogenetic distinctiveness from a common Demospongiae/Hexactinellida taxon. Both intraspecific and intraclass patterns of Calcarea showed great similarity, suggesting a conserved fatty acid composition that already existed in the last common ancestor of Calcinea and Calcaronea, i.e. before subclasses diverged.

Animals↗

Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA.

Calcareous sponges (Porifera, Calcarea) play an important role for our understanding of early metazoan evolution, since several molecular studies suggested their closer relationship to Eumetazoa than to the other two sponge 'classes,' Demospongiae and Hexactinellida. The division of Calcarea into the subtaxa Calcinea and Calcaronea is well established by now, but their internal relationships remain largely unresolved. Here, we estimate phylogenetic relationships within Calcarea in a Bayesian framework, using full-length 18S and partial 28S ribosomal DNA sequences. Both genes were analyzed separately and in combination and were further partitioned by stem and loop regions, the former being modelled to take non-independence of paired sites into account. By substantially increasing taxon sampling, we show that most of the traditionally recognized supraspecific taxa within Calcinea and Calcaronea are not monophyletic, challenging the existing classification system, while monophyly of Calcinea and Calcaronea is again highly supported.

Animals↗

Nano-cluster composite structure of calcitic sponge spicules--a case study of basic characteristics of biominerals.

Spicules of calcareous sponges are elaborately shaped skeletal elements that nonetheless show characteristics of calcite single-crystals. Our atomic force microscopic and transmission electron microscopic investigation of the triradiate spicules of the sponge Pericharax heteroraphis reveals a nano-cluster structure with mostly well-aligned small crystal domains and pockets with accumulated domain misalignments. Combined high-resolution and energy-filtering transmission electron microscopy revealed carbon enrichments located in between crystal domain boundaries, which strongly suggests an intercalated network-like proteinaceous organic matrix. This matrix is proposed to be involved in the nano-clustered calcite precipitation via a transient phase that may enable a 'brick-by-brick' formation of composite and yet single-crystalline spicules with elaborate morphologies. This composite cluster structure reduces the brittleness of the material by dissipating strain energy and deflecting crack propagation from the calcite cleavage planes, but the lattice symmetry and anisotropic growth properties of calcite still play a major role in the morphogenesis of these unusual calcite single-crystals. Our structural, crystallographic, textural, and chemical analysis of sponge spicules corroborates the view that nano-clustered crystal growth, induced by organic matrices, is a basic characteristic of biomineralisation that enables the production of composite materials with elaborate morphologies.

Animals↗

Intragenomic variation of the rDNA internal transcribed spacers in sponges (Phylum Porifera): implications for phylogenetic studies.

The internal transcribed spacer regions (ITS1 and ITS2) of the tandemly repeated nuclear ribosomal DNA clusters are frequently used as markers for fine scale analyses in diverse animals. In certain taxa, ITS is nearly exclusively used for population level or inter-specific studies, despite the frequent presence of divergent paralogs within individual genomes that can be phylogenetically misleading. For the first time we survey diverse marine sponges to determine the extent and phylogenetic implications of intragenomic polymorphisms (IGPs) exhibited at their ITS loci. We discover that the extent of IGP varies greatly between taxa (with most taxa exhibiting very few) and cannot be predicted by taxonomy. Furthermore, we demonstrate that ITS can be phylogenetically informative between species when moderate levels of IGPs are detected, but that ITS paralogy can interfere with population level studies. We caution against the routine use of ITS in phylogenetic studies of sponges without (1) screening for IGPs in specimens from every population sampled; (2) including all divergent paralogs in phylogenetic analyses; (3) testing ITS data using other single-copy, unlinked loci (such as nuclear introns).

Animals↗

A chemical view of the most ancient metazoa--biomarker chemotaxonomy of hexactinellid sponges.

Hexactinellid sponges are often considered to be the most ancient metazoans. Lipid biomarkers from 23 species were studied for information on their phylogenetic properties, particularly their disputed relation to the two other sponge classes (Demospongiae, Calcarea). The most prominent lipid compounds in the Hexactinellida comprise C28 to C32 polyenoic fatty acids. Their structures parallel the unique patterns found in demosponge membrane fatty acids ('demospongic acids') and strongly support a close phylogenetic association of the Demospongiae and the Hexactinellida. Both taxa also show unusual mid-chain methylated fatty acids (C15-C25) and irregular C25- and C40-isoprenoid hydrocarbons, tracers for specific eubacteria and Archaea, respectively. These biomarkers indicate a similar, highly conservative symbiont community, although some shift in the abundance of the associated microbiota was observed. The lack of these features in calcareous sponges further contradicts the still common view that Calcarea and Demospongiae are more closely related to each other than either is to the Hexactinellida.

Animals↗

Phylogeography of western Pacific Leucetta 'chagosensis' (Porifera: Calcarea) from ribosomal DNA sequences: implications for population history and conservation of the Great Barrier Reef World Heritage Area (Australia).

Leucetta 'chagosensis' is a widespread calcareous sponge, occurring in shaded habitats of Indo-Pacific coral reefs. In this study we explore relationships among 19 ribosomal DNA sequence types (the ITS1-5.8S-ITS2 region plus flanking gene sequences) found among 54 individuals from 28 locations throughout the western Pacific, with focus on the Great Barrier Reef (GBR). Maximum parsimony analysis revealed phylogeographical structuring into four major clades (although not highly supported by bootstrap analysis) corresponding to the northern/central GBR with Guam and Taiwan, the southern GBR and subtropical regions south to Brisbane, Vanuatu and Indonesia. Subsequent nested clade analysis (NCA) confirmed this structure with a probability of > 95%. After NCA of geographical distances, a pattern of range expansion from the internal Indonesian clade was inferred at the total cladogram level, as the Indonesian clade was found to be the internal and therefore oldest clade. Two distinct clades were found on the GBR, which narrowly overlap geographically in a line approximately from the Whitsunday Islands to the northern Swain Reefs. At various clade levels, NCA inferred that the northern GBR clade was influenced by past fragmentation and contiguous range expansion events, presumably during/after sea level low stands in the Pleistocene, after which the northern GBR might have been recolonized from the Queensland Plateau in the Coral Sea. The southern GBR clade is most closely related to subtropical L. 'chagosensis', and we infer that the southern GBR probably was recolonized from there after sea level low stands, based on our NCA results and supported by oceanographic data. Our results have important implications for conservation and management of the GBR, as they highlight the importance of marginal transition zones in the generation and maintenance of species rich zones, such as the Great Barrier Reef World Heritage Area.

Animals↗

Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity.

Demosponges are considered part of the most basal evolutionary lineage in the animal kingdom. Although the sponge body plan fundamentally differs from that of other metazoans, their development includes many of the hallmarks of bilaterian and eumetazoan embryogenesis, namely fertilization followed by a period of cell division yielding distinct cell populations, which through a gastrulation-like process become allocated into different cell layers and patterned within these layers. These observations suggest that the last common ancestor (LCA) to all living animals was developmentally more sophisticated than is widely appreciated and used asymmetric cell division and morphogen gradients to establish localized populations of specified cells within the embryo. Here we demonstrate that members of a range of transcription factor gene classes, many of which appear to be metazoan-specific, are expressed during the development of the demosponge Reniera, including ANTP, Pax, POU, LIM-HD, Sox, nuclear receptor, Fox (forkhead), T-box, Mef2, and Ets genes. Phylogenetic analysis of these genes suggests that not only the origin but the diversification of some of the major developmental metazoan transcription factor classes took place before sponges diverged from the rest of the Metazoa. Their expression during demosponge development suggests that, as in today's sophisticated metazoans, these genes may have functioned in the regulatory network of the metazoan LCA to control cell specification and regionalized gene expression during embryogenesis.

Amino Acid Sequence↗