John N. A. Hooper

Global Diversity of Sponges (Porifera)

With the completion of a single unified classification, the Systema Porifera (SP) and subsequent development of an online species database, the World Porifera Database (WPD), we are now equipped to provide a first comprehensive picture of the global biodiversity of the Porifera. An introductory overview of the four classes of the Porifera is followed by a description of the structure of our main source of data for this paper, the WPD. From this we extracted numbers of all ‘known’ sponges to date: the number of valid Recent sponges is established at 8,553, with the vast majority, 83%, belonging to the class Demospongiae. We also mapped for the first time the species richness of a comprehensive set of marine ecoregions of the world, data also extracted from the WPD. Perhaps not surprisingly, these distributions appear to show a strong bias towards collection and taxonomy efforts. Only when species richness is accumulated into large marine realms does a pattern emerge that is also recognized in many other marine animal groups: high numbers in tropical regions, lesser numbers in the colder parts of the world oceans. Preliminary similarity analysis of a matrix of species and marine ecoregions extracted from the WPD failed to yield a consistent hierarchical pattern of ecoregions into marine provinces. Global sponge diversity information is mostly generated in regional projects and resources: results obtained demonstrate that regional approaches to analytical biogeography are at present more likely to achieve insights into the biogeographic history of sponges than a global perspective, which appears currently too ambitious. We also review information on invasive sponges that might well have some influence on distribution patterns of the future.

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.

Biodiversity ‘hotspots’, patterns of richness and endemism, and taxonomic affinities of tropical Australian sponges (Porifera)

Abstract‘Hotspots’ of biodiversity (taxonomic richness, endemism, taxonomic affinities between communities) at small (α), medium (β) and larger (γ) scales of diversity were examined for marine sponge populations throughout tropical and subtropical Australia, with the faunas of Vanuatu, Palau and Thailand used as outgroups for comparison. Spatial and numerical (ordination) models and hierarchic classifications delineated 37 β and 13 γ scale faunas from 1343 investigated localities using a pool of 2324 species. The Australian taxonomic literature was ignored completely to avoid the many still unresolved taxonomic problems and to allow equal treatment of collecting localities. Richness and endemism varied considerably between marine areas, for species and genera at all spatial scales, with gradients strongly corroborated by hierarchic taxonomic relationships between faunas. Richness and endemism were equally effective indicators of biodiversity ‘hotspots’, whereas species-level vs. genus-level data produced differing patterns, with the latter substantially underestimating biodiversity and marine area relationships, and consequently a poor surrogate’ for species data. Patterns of taxa shared between adjacent areas were more informative than richness and endemism data alone, as they more accurately reflect the processes in these areas. Latitudinal gradients in sponge diversity were not evident, whereas various environmental factors were prominent at α scales and biogeographic factors were prominent at β and γ scales of diversity. An example of a small (α) scale diversity fauna revealed substantial spatial heterogeneity (mean of 41 spp/locality, 33% apparently endemic, and a total fauna of 226 spp) containing few ubiquitous species (40% or 78 spp), with adjacent reefs having relatively low faunal similarity (mean 33%). Faunas at the medium (β) scale of diversity were less heterogeneous (mean 127 spp/region, 27% apparently endemic to a particular region, with a total fauna of 2324 spp), containing a significantly larger dataset (829 spp) found in >1 region to assess taxonomic affinities. At the larger (γ) scale of diversity faunas were far more heterogeneous (mean 263 spp/region, 47% apparently endemic to a particular region) containing a smaller dataset (only 588 spp or 26% of the fauna with >1 species/region) to assess taxonomic affinities. Consequently, sponge faunas at the α and γ scales of diversity are ineffective and inappropriate as biodiversity models, respectively, with γ scale diversity also less relevant as a practical tool for marine resource management and marine area conservation.

Haliclonacyclamines A and B, cytotoxic alkaloids from the tropical marine sponge Haliclona sp

Abstract The structures of haliclonacyclamines A (1) and B (2), and their methiodide salts (3) and (4), were investigated by 1D- and 2D-NMR experiments, notably DQFCOSY, HMBC, HMQC-HOHAHA, and HOHAHA. The relative stereochemistry and position of alkene substituents were determined by single crystal x-ray study at low temperature. The parent haliclonacyclamines show pronounced cytotoxic, antibacterial and antifungal activity.

Clavatadine A, A Natural Product with Selective Recognition and Irreversible Inhibition of Factor XIa †

Bioassay-guided fractionation of a CH2Cl2/MeOH extract of the sponge Suberea clavata using the serine protease factor XIa to detect antithrombotic activity led to the isolation of the new marine natural products, clavatadines A and B. Clavatadines A and B inhibited factor XIa with IC50s of 1.3 and 27 microM, respectively. A crystal structure of protein-inhibitor (clavatadine A) complex was obtained and revealed interesting selective binding and irreversible inhibition of factor XIa. The cocrystal structure provides guidance for the design and synthesis of future factor XIa inhibitors as antithrombotic agents.

Towards a DNA taxonomy of Caribbean demosponges: a gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae

We present the most comprehensive cytochrome oxidase subunit 1 gene tree published to date for demosponges based on new sequences. The CO1 barcoding fragment is sequenced for 65 species from the Caribbean Sea, and its gene tree reconstructed. Although its deeper nodes are not particularly well-supported, the gene tree provides a variety of information for new phylogenetic patterns, as well as support for previously published 28S rDNA gene trees. In our analysis Halichondriidae cluster with Suberitidae, supporting previous 28S rDNA data. Chelae-bearing Poecilosclerida are monophyletic but most taxa lacking chelae in this dataset cluster more distantly. Haplosclerida are not resolved monophyletically under this fragment. While some species exhibit distinct barcodes, some genera contain species that share CO1 haplotypes.

Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks

Abstract Marine sponges are an ecologically important and highly diverse component of marine benthic communities, found in all the worlds oceans, at all depths. Although their commercial potential and evolutionary importance is increasingly recognized, many pivotal aspects of their basic biology remain enigmatic. Knowledge of historical biogeographic affinities and biodiversity patterns is rudimentary, and there are still few data about genetic variation among sponge populations and spatial patterns of this variation. Biodiversity analyses of tropical Australasian sponges revealed spatial trends not universally reflected in the distributions of other marine phyla within the Indo-West Pacific region. At smaller spatial scales sponges frequently form heterogeneous, spatially patchy assemblages, with some empirical evidence suggesting that environmental variables such as light and/or turbidity strongly contribute to local distributions. There are no apparent latitudinal diversity gradients at larger spatial scales but stochastic processes, such as changing current patterns, the presence or absence of major carbonate platforms and historical biogeography, may determine modern day distributions. Studies on Caribbean oceanic reefs have revealed similar patterns, only weakly correlated with environmental factors. However, several questions remain where molecular approaches promise great potential, e.g., concerning connectivity and biogeographic relationships. Studies to date have helped to reveal that sponge populations are genetically highly structured and that historical processes might play an important role in determining such structure. Increasingly sophisticated molecular tools are now being applied, with results contributing significantly to a better understanding of poriferan microevolutionary processes and molecular ecology.

Mutremdamide A and koshikamides C-H, peptide inhibitors of HIV-1 entry from different Theonella species.

A new sulfated cyclic depsipeptide, termed mutremdamide A, and six new highly N-methylated peptides, termed koshikamides C-H, were isolated from different deep-water specimens of Theonella swinhoei and Theonella cupola. Their structures were determined using extensive 2D NMR, ESI, or CDESI and QTOF-MS/MS experiments and absolute configurations established by quantum mechanical calculations, advanced Marfeys method, and chiral HPLC. Mutremdamide A displays a rare 2-amino-3-(2-hydroxyphenyl)propanoic acid and a new N(delta)-carbamoyl-beta-sulfated asparagine. Koshikamides C-E are linear undecapeptides, and koshikamides F-H are 17-residue depsipeptides containing a 10-residue macrolactone. Koshikamides F and G differ from B and H in part by the presence of the conjugated unit 2-(3-amino-5-oxopyrrolidin-2-ylidene)propanoic acid. Cyclic koshikamides F and H inhibited HIV-1 entry at low micromolar concentrations while their linear counterparts were inactive. The Theonella collections studied here are distinguished by co-occurrence of mutremdamide A, koshikamides, and theonellamides, the combination of which appears to define a new Theonella chemotype that can be found in deeper waters.

Revision of the family Raspailiidae (Porifera : Demospongiae), with description of Australian species

The marine sponge family Raspailiidae Hentschel is revised and referred to the order Poecilosclerida. Of 48 nominal genera, 17 (including one new genus and one new subgenus) are recognised here: Raspailia Nardo, (Hymeraphiopsis, subg. nov.), Ectyoplasia Topsent, Endectyon Topsent, Trikentrion Ehlers, Cyamon Gray, Aulospongus Norman, Raspaciona Topsent, Rhabdeurypon Topsent, Eurypon Gray, Plocamione Topsent, Amphinomia, gen. nov., Lithoplocamia Dendy, Hymeraphia Bowerbank, Ceratopsion Strand, Thrinacophora Ridley, Axechina Hentschel and Echinodictyum Ridley, and three genera are incertae sedis (Tethyspira Topsent, Sigmeurypon Topsent, Cantabrina Ferrer-Hernandez). Fifty-six species are described for the Australian fauna, of which 14 are new to science: Raspailia daminensis, R. desrnonyiformis, R. keriontria, R. melanorhops, R. phakellopsis, R. reticulata, R. wardi, R. wilkinsoni, Ectyoplasia vannus, Endectyon elyakovi, Ceratopsion montebelloensis, C. palmafa, Echinodictyum austrinus, spp. nov. and Amphinomia sulphurea, gen. nov., sp. nov. The phylogenetic relationships and biogeographical distribution of the family are discussed. Tropical north-westem Australian-southem Indonesia has the highest diversity of species in the Indo-west Pacific, and altogether the Australasian region has about 20% of the worlds known raspailiid fauna.

CO I barcoding reveals new clades and radiation patterns of Indo-Pacific sponges of the family Irciniidae (Demospongiae: Dictyoceratida).

Background DNA barcoding is a promising tool to facilitate a rapid and unambiguous identification of sponge species. Demosponges of the order Dictyoceratida are particularly challenging to identify, but are of ecological as well as biochemical importance. Methodology/Principal Findings Here we apply DNA barcoding with the standard CO1-barcoding marker on selected Indo-Pacific specimens of two genera, Ircinia and Psammocinia of the family Irciniidae. We show that the CO1 marker identifies several species new to science, reveals separate radiation patterns of deep-sea Ircinia sponges and indicates dispersal patterns of Psammocinia species. However, some species cannot be unambiguously barcoded by solely this marker due to low evolutionary rates. Conclusions/Significance We support previous suggestions for a combination of the standard CO1 fragment with an additional fragment for sponge DNA barcoding.