Manuel Maldonado

Decline in Mesozoic reef-building sponges explained by silicon limitation

Several unrelated clades of siliceous sponges proliferated on the shelves of the Jurassic Tethys Sea, becoming prominent builders in reefs and near-shore mounds. Many of these builders are characterized by massive, rock-like skeletons made of spicules with a characteristic terminal hypersilicification. Such hypertrophied spicules are generically known as desmas, irrespective of their phylogenetic origin. Desma-bearing sponges virtually disappeared from reefs and other neritic environments during the Cretaceous and the Early Tertiary, but have subsisted in relict populations in deeper, bathyal waters. The causes of the decline and bathymetric shift of these sponges remain obscure. Here we show experimentally that the concentration of silicic acid in seawater modulates the phenotypic expression of the various spicule types genetically available in a sponge species. We also show that the concentration of this nutrient in Recent surface waters is insufficient for this species to secrete its desmas. These findings indicate that silicon limitation, probably aggravated in shallow waters by the diatom burst around the Cretaceous–Tertiary boundary, may have forced neritic sponges with desmas to either lighten their skeletons or move to deeper, silicon-rich environments.

Deep metazoan phylogeny: When different genes tell different stories

Molecular phylogenetic analyses have produced a plethora of controversial hypotheses regarding the patterns of diversification of non-bilaterian animals. To unravel the causes for the patterns of extreme inconsistencies at the base of the metazoan tree of life, we constructed a novel supermatrix containing 122 genes, enriched with non-bilaterian taxa. Comparative analyses of this supermatrix and its two non-overlapping multi-gene partitions (including ribosomal and non-ribosomal genes) revealed conflicting phylogenetic signals. We show that the levels of saturation and long branch attraction artifacts in the two partitions correlate with gene sampling. The ribosomal gene partition exhibits significantly lower saturation levels than the non-ribosomal one. Additional systematic errors derive from significant variations in amino acid substitution patterns among the metazoan lineages that violate the stationarity assumption of evolutionary models frequently used to reconstruct phylogenies. By modifying gene sampling and the taxonomic composition of the outgroup, we were able to construct three different yet well-supported phylogenies. These results show that the accuracy of phylogenetic inference may be substantially improved by selecting genes that evolve slowly across the Metazoa and applying more realistic substitution models. Additional sequence-independent genomic markers are also necessary to assess the validity of the phylogenetic hypotheses.

Nutrient fluxes through sponges: biology, budgets, and ecological implications.

Marine sponges are able to process a variety of carbon (C), nitrogen (N), phosphorous (P), and silicon (Si) dissolved compounds, in addition to the particulate C, N, and P obtained through regular feeding. While Si fluxes through sponges are exclusively related to the elaboration of their skeleton of biogenic silica, C, N, and P fluxes derive from a complex combination of metabolic processes that include feeding, respiration, egestion, excretion, as well as hosting of large microbial populations within the sponge body. Because of the remarkable abundance of sponges in many benthic marine communities, they have the potential to impact the availability of the compounds they take up and release, affecting the benthic-pelagic coupling and cycling rates of chemical elements that are crucial to determine growth of bacterioplankton and primary producers at the ecosystem level. Unfortunately, our knowledge and understanding of the magnitude of the sponge-meditated nutrient fluxes and their ecological implications depends much on the compound type (i.e. C, N, P, or Si). Herein, we review the available knowledge on the subject with emphasis on recent developments.

Three-dimensional chitin-based scaffolds from Verongida sponges (Demospongiae: Porifera). Part I. Isolation and identification of chitin.

Marine invertebrate organisms including sponges (Porifera) not only provide an abundant source of biologically active secondary metabolites but also inspire investigations to develop biomimetic composites, scaffolds and templates for practical use in materials science, biomedicine and tissue engineering. Here, we presented a detailed study of the structural and physico-chemical properties of three-dimensional skeletal scaffolds of the marine sponges Aiolochroia crassa, Aplysina aerophoba, A. cauliformis, A. cavernicola, and A. fulva (Verongida: Demospongiae). We show that these fibrous scaffolds have a multilayered design and are made of chitin. (13)C solid-state NMR spectroscopy, NEXAFS, and IR spectroscopy as well as chitinase digestion and test were applied in order to unequivocally prove the existence of alpha-chitin in all investigated species.

Nutrient Fluxes Through Sponges

Marine sponges are able to process a variety of carbon (C), nitrogen (N), phosphorous (P), and silicon (Si) dissolved compounds, in addition to the particulate C, N, and P obtained through regular feeding. While Si fluxes through sponges are exclusively related to the elaboration of their skeleton of biogenic silica, C, N, and P fluxes derive from a complex combination of metabolic processes that include feeding, respiration, egestion, excretion, as well as hosting of large microbial populations within the sponge body. Because of the remarkable abundance of sponges in many benthic marine communities, they have the potential to impact the availability of the compounds they take up and release, affecting the benthic-pelagic coupling and cycling rates of chemical elements that are crucial to determine growth of bacterioplankton and primary producers at the ecosystem level. Unfortunately, our knowledge and understanding of the magnitude of the sponge-meditated nutrient fluxes and their ecological implications depends much on the compound type (i.e. C, N, P, or Si). Herein, we review the available knowledge on the subject with emphasis on recent developments.

Deep phylogeny and evolution of sponges (phylum Porifera).

Sponges (phylum Porifera) are a diverse taxon of benthic aquatic animals of great ecological, commercial, and biopharmaceutical importance. They are arguably the earliest-branching metazoan taxon, and therefore, they have great significance in the reconstruction of early metazoan evolution. Yet, the phylogeny and systematics of sponges are to some extent still unresolved, and there is an on-going debate about the exact branching pattern of their main clades and their relationships to the other non-bilaterian animals. Here, we review the current state of the deep phylogeny of sponges. Several studies have suggested that sponges are paraphyletic. However, based on recent phylogenomic analyses, we suggest that the phylum Porifera could well be monophyletic, in accordance with cladistic analyses based on morphology. This finding has many implications for the evolutionary interpretation of early animal traits and sponge development. We further review the contribution that mitochondrial genes and genomes have made to sponge phylogenetics and explore the current state of the molecular phylogenies of the four main sponge lineages (Classes), that is, Demospongiae, Hexactinellida, Calcarea, and Homoscleromorpha, in detail. While classical systematic systems are largely congruent with molecular phylogenies in the class Hexactinellida and in certain parts of Demospongiae and Homoscleromorpha, the high degree of incongruence in the class Calcarea still represents a challenge. We highlight future areas of research to fill existing gaps in our knowledge. By reviewing sponge development in an evolutionary and phylogenetic context, we support previous suggestions that sponge larvae share traits and complexity with eumetazoans and that the simple sedentary adult lifestyle of sponges probably reflects some degree of secondary simplification. In summary, while deep sponge phylogenetics has made many advances in the past years, considerable efforts are still required to achieve a comprehensive understanding of the relationships among and within the main sponge lineages to fully appreciate the evolution of this extraordinary metazoan phylum.

Sexual propagation by sponge fragments

Habitat fragmentation means that many species occur in discrete populations, so it is important for sessile species to colonize new areas. It has not been clear how sponges whose larvae disperse over short distances achieve this. Fragments may break off sponges as a result of physical and biological disturbance and are then dispersed by currents and recruited as independent individuals or colonies,. Local populations are expected to have high genetic relatedness as a result, but most sponge populations have high levels of genetic variability,. We suggest that this discrepancy results from an interaction between fragmentation and sexual reproduction.

Effects of the duration of larval life on postlarval stages of the demosponge Sigmadocia caerulea

Variability in the duration of the free-swimming period of lecithotrophic larvae of the demosponge Sigmadocia caerulea (Hechtel, 1965) was assessed in the laboratory in the absence of metamorphic inducers and inhibitors. The free-swimming period in three clutches of larvae ranged from 8 to 70 h and the cumulative settlement curve was sigmoid, with settlement peaking between 20 and 28 h after release. There were significant differences among clutches in the time to reach 50% settlement. Within each clutch, small percentages of larvae (<25%) were short-lived (settled less than 12 h after release) or long-lived (settling more than 32 h after release). Juveniles originating from short-lived larvae survived better, grew faster and were more regular in shape than those originating from long-lived larvae. In additional laboratory experiments, we examined the consequences of feeding during the early postsettlement period. Size differences between fed and starved juveniles became apparent 5 days after osculum formation, suggesting that the filter-feeding ability does not begin immediately after osculum formation. Our results are consistent with the hypothesis that long-lived larvae bring fewer reserves to the postsettlement period than do short-lived larvae, thereby experiencing nutritional stress prior to the onset of feeding that can reduce the vigor of the juveniles. Although larvae delaying metamorphosis should theoretically be important in colonizing new habitats and increasing gene flow, low postsettlement survival of such individuals may reduce the evolutionary importance of variability in the duration of the larval period.

Three-dimensional chitin-based scaffolds from Verongida sponges (Demospongiae: Porifera). Part II: Biomimetic potential and applications

In order to evaluate the biomedical potential of three-dimensional chitinous scaffolds of poriferan origin, chondrocyte culturing experiments were performed. It was shown for the first time that freshly isolated chondrocytes attached well to the chitin scaffold and synthesized an extracellular matrix similar to that found in other cartilage tissue engineering constructs. Chitin scaffolds also supported deposition of a proteoglycan-rich extracellular matrix of chondrocytes seeded bioconstructs in an in vivo environment. We suggest that chitin sponge scaffolds, apart from the demonstrated biomedical applications, are highly optimized structures for use as filtering systems, templates for biomineralization as well as metallization in order to produce catalysts.

Endosymbiotic Yeast Maternally Transmitted in a Marine Sponge

The detection of an endosymbiotic yeast in demosponges of the genus Chondrilla described here records the first such association within the phylum Porifera. The symbiont, interpreted as a yolk body in previous ultrastructural studies, is a chitinous-walled fission yeast. Chitin was detected by an immunocytochemical technique that labels its β-1,4-N-acetyl-d-glucosamine residues. Abundant symbiotic yeast cells (4.4 ± 2.3 cells per 10 μm2) transmitted from the soma through the oocytes to the fertilized eggs are directly propagated by vertical transmission in the female. Vertically transmitted yeast were detected in three Chondrilla species with disjunct biogeographical distributions: the Mediterranean, the Caribbean, and the Australian Pacific. Apparently these yeasts are not present in other demosponge genera. Therefore, the fungal endosymbiosis most likely evolved before or during the diversification of the genus Chondrilla.