Volcanic ash supports a diverse bacterial community in a marine mesocosm.

Shallow-water coral reef ecosystems, particularly those already impaired by anthropogenic pressures, may be highly sensitive to disturbances from natural catastrophic events, such as volcanic eruptions. Explosive volcanic eruptions expel large quantities of silicate ash particles into the atmosphere, which can disperse across millions of square kilometres and deposit into coral reef ecosystems. Following heavy ash deposition, mass mortality of reef biota is expected, but little is known about the recovery of post-burial reef ecosystems. Reef regeneration depends partly upon the capacity of the ash deposit to be colonised by waterborne bacterial communities and may be influenced to an unknown extent by the physiochemical properties of the ash substrate itself. To determine the potential for volcanic ash to support pioneer bacterial colonisation, we exposed five well-characterised volcanic and coral reef substrates to a marine aquarium under low light conditions for 3 months: volcanic ash, synthetic volcanic glass, carbonate reef sand, calcite sand and quartz sand. Multivariate statistical analysis of Automated Ribosomal Intergenic Spacer Analysis (ARISA) fingerprinting data demonstrates clear segregation of volcanic substrates from the quartz and coral reef substrates over 3 months of bacterial colonisation. Overall bacterial diversity showed shared and substrate-specific bacterial communities; however, the volcanic ash substrate supported the most diverse bacterial community. These data suggest a significant influence of substrate properties (composition, granulometry and colour) on bacterial settlement. Our findings provide first insights into physicochemical controls on pioneer bacterial colonisation of volcanic ash and highlight the potential for volcanic ash deposits to support bacterial diversity in the aftermath of reef burial, on timescales that could permit cascading effects on larval settlement.

Managing and sharing the escalating number of sponge "unknowns": the SpongeMaps project.

Contemporary collections of sponges in the Indo-west Pacific have escalated substantially due to pharmaceutical discovery, national bioregional planning, and compliance with international conventions on the seabed and its marine genetic resources beyond national jurisdictions. These partially processed operational taxonomic unit (OTU) collections now vastly outweigh the expertise available to make them better "known" via complete taxonomy, yet for many bioregions they represent the most significant body of currently available knowledge. Increasing numbers of cryptic species, previously undetected morphologically, are now being discovered by molecular and chemical analyses. The uncoordinated and fragmented nature of many previous collections, however, means that knowledge and expertise gained from a particular project are often lost to future projects without a biodiversity informatics legacy. Integrating these diverse data (GIS; OTUs; images; molecular, chemical, and other datasets) required a two-way iterative process so far unavailable for sponges with existing biodiversity informatics tools. SpongeMaps arose from the initial need for online collaboration to integrate morphometric data with molecular barcodes, including the Porifera Tree of Life (PorTol) project. It provides interrogation of existing data to better process new collections; capacity to create new OTUs; publication of online pages for individual species, so as to interpret GIS and other data for online biodiversity databases and services; and automatic links to external datasets for taxonomic hierarchy, specimen GIS and mapping, DNA sequence data, chemical structures, and images.

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.

NUMTs in the sponge genome reveal conserved transposition mechanisms in metazoans.

The transposition of parts of the mitochondrial (mt) genetic material into the nuclear genome (NUMTs) occurs in a wide range of eukaryotes. Here, we show that NUMTs exist for nearly all regions of the mt genome in the demosponge Amphimedon queenslandica, a representative of the oldest phyletic lineage of animals. Because the sponge NUMTs are small and noncoding, and transposed via a DNA intermediate, as in eumetazoans, we infer that the transpositonal processes underlying NUMT formation in contemporary animals existed in their most recent common ancestor. In contrast to most bilaterians, Amphimedon NUMTs are inserted into regions of high gene density. Given the common features of metazoan NUMTs, the reduction in animal mt genome sizes relative to other eukaryotes may be the product of the mt DNA transposition mechanisms that evolved along the metazoan stem.

Poriferan survivin exhibits a conserved regulatory role in the interconnected pathways of cell cycle and apoptosis.

Survivin orchestrates intracellular pathways during cell division and apoptosis. Its central function as mitotic regulator and inhibitor of cell death has major implications for tumor cell proliferation. Analyses in early-branching Metazoa so far propose an exclusive role of survivin as a chromosomal passenger protein, whereas only later during evolution a complementary antiapoptotic function might have arisen, concurrent with increased organismal complexity. To lift the veil on the ancestral function(s) of this key regulator, a survivin-like protein (SURVL) of one of the earliest-branching metazoan taxa was identified and functionally characterized. SURVL of the sponge Suberites domuncula shares considerable similarities with its metazoan homologs, ranging from conserved exon/intron structure to presence of protein-interaction domains. Whereas sponge tissue shows a low steady-state level, SURVL expression was significantly upregulated in rapidly proliferating primmorph cells. In addition, challenge of tissue and primmorphs with heavy metal or lipopeptide stimulated SURVL expression, concurrent with the expression of a newly discovered caspase. Complementary functional analyses in transfected HEK-293 cells revealed that heterologous expression of a SURVL-EFGP fusion not only promotes proliferation but also enhances resistance to cadmium-induced cell death. Taken together, these results suggest both a deep evolutionary conserved dual role of survivin and an equally conserved central position in the interconnected pathways of cell cycle and apoptosis.

Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships.

Despite expanding data sets and advances in phylogenomic methods, deep-level metazoan relationships remain highly controversial. Recent phylogenomic analyses depart from classical concepts in recovering ctenophores as the earliest branching metazoan taxon and propose a sister-group relationship between sponges and cnidarians (e.g., Dunn CW, Hejnol A, Matus DQ, et al. (18 co-authors). 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745-749). Here, we argue that these results are artifacts stemming from insufficient taxon sampling and long-branch attraction (LBA). By increasing taxon sampling from previously unsampled nonbilaterians and using an identical gene set to that reported by Dunn et al., we recover monophyletic Porifera as the sister group to all other Metazoa. This suggests that the basal position of the fast-evolving Ctenophora proposed by Dunn et al. was due to LBA and that broad taxon sampling is of fundamental importance to metazoan phylogenomic analyses. Additionally, saturation in the Dunn et al. character set is comparatively high, possibly contributing to the poor support for some nonbilaterian nodes.

An evolutionary fast-track to biocalcification.

The ability to construct mineralized shells, spicules, spines and skeletons is thought to be a key factor that fuelled the expansion of multicellular animal life during the early Cambrian. The genes and molecular mechanisms that control the process of biomineralization in disparate phyla are gradually being revealed, and it is broadly recognized that an insoluble matrix of proteins, carbohydrates and other organic molecules are required for the initiation, regulation and inhibition of crystal growth. Here, we show that Astrosclera willeyana, a living representative of the now largely extinct stromatoporid sponges (a polyphyletic grade of poriferan bauplan), has apparently bypassed the requirement to evolve many of these mineral-regulating matrix proteins by using the degraded remains of bacteria to seed CaCO(3) crystal growth. Because stromatoporid sponges formed extensive reefs during the Paelozoic and Mesozoic eras (fulfilling the role that stony corals play in modern coral reefs), and fossil evidence suggests that the same process of bacterial skeleton formation occurred in these stromatoporid ancestors, we infer that some ancient reef ecosystems might have been founded on this microbial-metazoan relationship.

Mitochondrial diversity of early-branching metazoa is revealed by the complete mt genome of a haplosclerid demosponge.

The first mitochondrial (mt) genomes of demosponges have recently been sequenced and appear to be markedly different from published eumetazoan mt genomes. Here we show that the mt genome of the haplosclerid demosponge Amphimedon queenslandica has features that it shares with both demosponges and eumetazoans. Although the A. queenslandica mt genome has typical demosponge features, including size, long noncoding regions, and bacterialike rRNA genes, it lacks atp9, which is found in the other demosponges sequenced to date. We found strong evidence of a recent transposon-mediated transfer of atp9 to the nuclear genome. In addition, A. queenslandica bears an incomplete tRNA set, unusual amino acid deletion patterns, and a putative control region. Furthermore, the arrangement of mt rRNA genes differs from that of other demosponges. These genes evolve at significantly higher rates than observed in other demosponges, similar to previously observed nuclear rRNA gene rates in other haplosclerid demosponges.

Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria).

Mitochondrial genes have been used extensively in population genetic and phylogeographical analyses, in part due to a high rate of nucleotide substitution in animal mitochondrial DNA (mtDNA). Nucleotide sequences of anthozoan mitochondrial genes, however, are virtually invariant among conspecifics, even at third codon positions of protein-coding sequences. Hence, mtDNA markers are of limited use for population-level studies in these organisms. Mitochondrial gene sequence divergence among anthozoan species is also low relative to that exhibited in other animals, although higher level relationships can be resolved with these markers. Substitution rates in anthozoan nuclear genes are much higher than in mitochondrial genes, whereas nuclear genes in other metazoans usually evolve more slowly than, or similar to, mitochondrial genes. Although several mechanisms accounting for a slow rate of sequence evolution have been proposed, there is not yet a definitive explanation for this observation. Slow evolution and unique characteristics may be common in primitive metazoans, suggesting that patterns of mtDNA evolution in these organisms differ from that in other animal systems.