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Staff Publications

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    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

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Seasonal Variation of Fatty Acids and Stable Carbon Isotopes in Sponges as Indicators for Nutrition: Biomarkers in Sponges Identified
Koopmans, M. ; Rijswijk, P. van; Boschker, H.T.S. ; Houtekamer, M. ; Martens, D.E. ; Wijffels, R.H. - \ 2015
Marine Biotechnology 17 (2015)1. - ISSN 1436-2228 - p. 43 - 54.
marine organisms - halichondria-panicea - lipids - sea - demospongiae - community - bacteria
To get a better understanding of sponge feeding biology and efficiencies, the fatty acid (FA) composition and 13C natural abundance of sponges and of suspended particulate matter (SPM) from surrounding seawater was studied in different seasons at three locations. Haliclona oculata and Haliclona xena from the Oosterschelde, the Netherlands, Halichondria panicea and H. xena from Lake Veere, the Netherlands, and Aplysina aerophoba and Dysidea avara from the Mediterranean, Spain, were studied. Several FA biomarkers for different algal groups, bacteria and sponge biomass were identified in all sponges. The FA concentration variation in sponges was related to changes in fatty acid concentration in SPM. Stable carbon isotopic ratios (d13C) in sponge specific FAs showed very limited seasonal variation at all sites. Algal FAs in sponges were mainly acquired from the SPM through active filtration in all seasons. At the two sites in the Netherlands only in May (spring), the sponge specific FAs had similar d13C ratios as algal FAs, suggesting that sponges were mainly growing during spring and probably summer. During autumn and winter, they were still actively filtering, but the food collected during this period had little effect on sponge d13C values suggesting limited incorporation of filtered material into the sponge body. The sponge A. aerophoba relied mostly on the symbiotic bacteria. In conclusion, fatty acid composition in combination with stable carbon isotope analysis can be used to analyze the food source of sponges.
Cell Turnover and Detritus Production in Marine Sponges from Tropical and Temperate Benthic Ecosystems
Alexander, B.E. ; Liebrand, K. ; Osinga, R. ; Geest, H.G. van der; Admiraal, W. ; Cleutjens, J.P.M. ; Schutte, B. ; Verheyen, F. ; Ribes, M. ; Loon, E. van; Goeij, J.M. de - \ 2014
PLoS One 9 (2014)10. - ISSN 1932-6203 - 11 p.
fresh-water sponge - stem-cells - ephydatia-fluviatilis - intestinal epithelium - tissue homeostasis - coral-reefs - in-vitro - demospongiae - cycle - population
This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-2'-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1±15.9% and 19.0±2.0% choanocyte proliferation (mean±SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.6±3.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.1±3.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.5±6.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8–73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5–18% detritus bodyweight-1·d-1) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs.
Deep-water sponges (Porifera) from Bonaire and Klein Curacao, Southern Caribbean
Soest, R.W.M. ; Meesters, H.W.G. ; Becking, L.E. - \ 2014
Zootaxa 3878 (2014)5. - ISSN 1175-5326 - p. 401 - 443.
southwestern atlantic - brazilian coast - coral-reefs - demospongiae - plakinidae
Four submersible dives off the coast of Bonaire (Caribbean Netherlands) and Klein Curaçao (Curaçao) to depths of 99.5–242 m, covering lower mesophotic and upper dysphotic zones, yielded 52 sponge specimens belonging to 31 species. Among these we identified 13 species as new to science. These are Plakinastrella stinapa n. sp., Pachastrella pacoi n. sp., Characella pachastrelloides n. sp., Geodia curacaoensis n. sp., Caminus carmabi n. sp., Discodermia adhaerens n. sp., Clathria (Microciona) acarnoides n. sp., Antho (Acarnia) pellita n. sp., Parahigginsia strongylifera n. sp., Calyx magnoculata n. sp., Neopetrosia dutchi n. sp., Neopetrosia ovata n. sp. and Neopetrosia eurystomata n. sp. We also report an euretid hexactinellid, which belongs to the rare genus Verrucocoeloidea, recently described (2014) as V. liberatorii Reiswig & Dohrmann. The remaining 18 already known species are all illustrated by photos of the habit, either in situ or ‘on deck’, but only briefly characterized in an annotated table to confirm their occurrence in the Southern Caribbean. The habitat investigated—steep limestone rocks, likely representing Pleistocene fossil reefs—is similar to deep-water fossil reefs at Barbados of which the sponges were sampled and studied by Van Soest and Stentoft (1988). A comparison is made between the two localities, showing a high degree of similarity in sponge composition: 53% of the present Bonaire-Klein Curaçao species were also retrieved at Barbados. At the level of higher taxa (genera, families) Bonaire-Klein Curaçao shared approximately 80% of its lower mesophotic and upper dysphotic sponge fauna with Barbados, despite a distance between them of 1000 km, indicating high faunal homogeneity. We also preliminarily compared the shallow-water (euphotic) sponge fauna of Curaçao with the combined data available for the Barbados, Bonaire and Klein Curaçao mesophotic and upper dysphotic sponges, which resulted in the conclusion that the two faunas show only little overlap.
Phylogeography of the Sponge Suberites diversicolor in Indonesia: Insights into the Evolution of Marine Lake Populations
Becking, L.E. ; Erpenbeck, D. ; Peijnenburg, K.T.C.A. ; Voogd, N.J. de - \ 2013
PLoS One 8 (2013)10. - ISSN 1932-6203
oxidase subunit-i - coral triangle - halocaridina-rubra - ribosomal dna - indo-pacific - life-history - porifera - biodiversity - islands - demospongiae
The existence of multiple independently derived populations in landlocked marine lakes provides an opportunity for fundamental research into the role of isolation in population divergence and speciation in marine taxa. Marine lakes are landlocked water bodies that maintain a marine character through narrow submarine connections to the sea and could be regarded as the marine equivalents of terrestrial islands. The sponge Suberites diversicolor (Porifera: Demospongiae: Suberitidae) is typical of marine lake habitats in the Indo-Australian Archipelago. Four molecular markers (two mitochondrial and two nuclear) were employed to study genetic structure of populations within and between marine lakes in Indonesia and three coastal locations in Indonesia, Singapore and Australia. Within populations of S. diversicolor two strongly divergent lineages (A & B) (COI: p = 0.4% and ITS: p = 7.3%) were found, that may constitute cryptic species. Lineage A only occurred in Kakaban lake (East Kalimantan), while lineage B was present in all sampled populations. Within lineage B, we found low levels of genetic diversity in lakes, though there was spatial genetic population structuring. The Australian population is genetically differentiated from the Indonesian populations. Within Indonesia we did not record an East-West barrier, which has frequently been reported for other marine invertebrates. Kakaban lake is the largest and most isolated marine lake in Indonesia and contains the highest genetic diversity with genetic variants not observed elsewhere. Kakaban lake may be an area where multiple putative refugia populations have come into secondary contact, resulting in high levels of genetic diversity and a high number of endemic species
Carbon conversion and metabolic rate in two marine sponges
Koopmans, M. ; Rijswijk, P. van; Martens, D.E. ; Egorova-Zachernyuk, T.A. ; Middelburg, J.J. ; Wijffels, R.H. - \ 2011
Marine Biology 158 (2011)1. - ISSN 0025-3162 - p. 9 - 20.
fatty-acids - stable-isotopes - organic-carbon - demospongiae - growth - lipids - invertebrates - regeneration - biomarkers - porifera
The carbon metabolism of two marine sponges, Haliclona oculata and Dysidea avara, has been studied using a 13C isotope pulse-chase approach. The sponges were fed 13C-labeled diatoms (Skeletonema costatum) for 8 h and they took up between 75 and 85%. At different times, sponges were sampled for total 13C enrichment, and fatty acid (FA) composition and 13C enrichment. Algal biomarkers present in the sponges were highly labeled after feeding but their labeling levels decreased until none was left 10 days after enrichment. The sponge-specific FAs incorporated 13C label already during the first day and the amount of 13C label inside these FAs kept increasing until 3 weeks after labeling. The algal-derived carbon captured by the sponges during the 8-h feeding period was thus partly respired and partly metabolized during the weeks following. Apparently, sponges are able to capture enough food during short periods to sustain longer-term metabolism. The change of carbon metabolic rate of fatty acid synthesis due to mechanical damage of sponge tissue was studied by feeding sponges with 13C isotope–labeled diatom (Pheaodactylum tricornutum) either after or before damaging and tracing back the 13C content in the damaged and healthy tissue. The filtration and respiration in both sponges responded quickly to damage. The rate of respiration in H. oculata reduced immediately after damage, but returned to its initial level after 6 h. The 13C data revealed that H. oculata has a higher metabolic rate in the tips where growth occurs compared to the rest of the tissue and that the metabolic rate is increased after damage of the tissue. For D. avara, no differences were found between damaged and non-damaged tissue. However, the filtration rate decreased directly after damage.
Heterogeneous oxygenation resulting from active and passive flow in two Mediterranean sponges, Dysidea avara and Chondrosia reniformis
Schlappy, M.L. ; Weber, M. ; Mendola, D. ; Hoffmann, F. ; Beer, D. de - \ 2010
Limnology and Oceanography 55 (2010)3. - ISSN 0024-3590 - p. 1289 - 1300.
marine sponges - aplysina-aerophoba - dynamics - demospongiae - microsensor - reduction - diversity
The oxygen dynamics and pumping behavior in Dysidea avara and Chondrosia reniformis (Porifera, Demospongiae) were investigated using oxygen microelectrodes and heated thermistor flow sensors. Both field and laboratory experiments showed the common occurrence of low oxygenation approaching anoxia in both species, lasting up to 1 h. Strong temporal and spatial heterogeneity of oxygen concentrations were observed with replicate oxygen profile series across the sponge surface, though tissue close to an osculum was generally better oxygenated than deeper in the sponge body. Because of observed lag times between a pumping event and the respective oxygenation response, the state of oxygenation of sponge tissue could only be partially attributed to its pumping activity. Ambient flow also influenced oxygenation patterns of sponges. Larger individuals possessing a functional aquiferous system regulated their pumping activity according to the ambient flow regime, whereas a small D. avara sponge, yet to possess its first osculum, was passively oxygenated by ambient flow and became anoxic approximately 30 min after ambient flow was stopped in its laboratory tank. These studies showed (1) sponge tissue metabolism switched frequently from aerobic to anaerobic, (2) temporally and spatially dynamic oxygen-depleted regions were commonly found within those sponges, both in captivity and in the field, and (3) tissue oxygenation was regulated both by active behavior (pumping) and passive environmental events (ambient water flow). We concluded that the metabolism of both sponge cells and sponge microbes will be influenced by the sponges' ability to control oxygen concentrations in different regions of its body at any particular time. In addition, when a sponge is actively pumping in a particular region of its body, higher oxygen concentrations will favor aerobic symbionts and aerobic metabolism, whereas when active pumping ceases, anaerobic symbionts and anaerobic tissue metabolism will be favored.
Spatial distribution of bacteria associated with the marine sponge Tethya californiana
Sipkema, D. ; Blanch, H.W. - \ 2010
Marine Biology 157 (2010)3. - ISSN 0025-3162 - p. 627 - 638.
microbial community - aplysina-aerophoba - ribosomal-rna - antimicrobial activity - phylogenetic analysis - diversity - demospongiae - alignments - symbionts - porifera
Microbial diversity and spatial distribution of the diversity within tissue of the marine sponge Tethya californiana was analyzed based on 16S rRNA gene sequences. One candidate division and nine bacterial phyla were detected, including members of all five subdivisions of Proteobacteria. Moreover, chloroplast-derived Stramenopiles- and Rhodophyta-affiliated 16S rRNA gene sequences were found and Stramenopiles represented the most abundant clones (30%) in the clone library. On the phylum-level, the microbial fingerprint of T. californiana showed a similar pattern as its Mediterranean relative T. aurantium. An interesting difference was that Cyanobacteria that were abundantly present in T. aurantium were not found in T. californiana, but that the latter sponges harbored phototrophic Stramenopiles instead. Surprisingly, the phototrophic microorganisms were evenly distributed over the inner and outer parts of the sponge tissue, which implies that they also reside in regions without direct light exposure. The other phyla were also present in both the outer cortex and the mesohyl of the sponges. These results were confirmed by analysis on the operational taxonomic unit level. This leads to the conclusion that from a qualitative point of view, spatial distribution of microorganisms in T. californiana tissue is quite homogeneous. Thirty-two percent of the operational taxonomic units shared less than 95% similarity with any other known sequence. This indicates that marine sponges are a rich source of previously undetected microbial life
Growth Efficiency and Carbon Balance for the Sponge Haliclona oculata
Koopmans, M. ; Martens, D.E. ; Wijffels, R.H. - \ 2010
Marine Biotechnology 12 (2010)3. - ISSN 1436-2228 - p. 340 - 349.
coral-reef sponge - halichondria-panicea - organic-carbon - oxygen-consumption - marine sponges - kiel bight - demospongiae - bacteria - filtration - retention
To obtain more knowledge about carbon requirements for growth by sponges, the growth rate, respiration rate, and clearance rate was measured in situ in Haliclona oculata. We found that only 34% of the particulate carbon pumped through the sponge was used for both respiration and growth. The net growth efficiency, being the ratio of carbon incorporated in biomass and the total carbon used by the sponge for respiration and growth, was found to be 0.099¿±¿0.013. Thus, about 10% of the total used carbon was fixed in biomass, and over 90% was used for generating energy for growth, maintenance, reproduction, and pumping. H. oculata had 2.5 µmol C available for every micromole O2 consumed. A value of 0.75 for respiratory quotient (RQ in micromole CO2 micromole O2-1) was used for H. oculata, which is the average value reported in literature for different marine invertebrates. Thus, carbon was available in excess to meet the respiratory demand. Oxygen was found not to be the limiting factor for growth, since only 3.3% of the oxygen pumped through the sponge body was used. Our results indicate that both oxygen and carbon availability are not limiting. The low growth efficiency agrees with the low growth rates found for the species used in this study
Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding
Goeij, J.M. de; Kluijver, A. de; Duyl, F.C. van; Vacelet, J. ; Wijffels, R.H. ; Goeij, A.F.P.M. de; Cleutjens, J.P.M. ; Schutte, B. - \ 2009
Journal of Experimental Biology 212 (2009)23. - ISSN 0022-0949 - p. 3892 - 3900.
organic-carbon doc - telomerase activity - suspension feeders - hydra-attenuata - cycle kinetics - iv collagen - porifera - demospongiae - removal - death
This study reveals the peculiar in vivo cell kinetics and cell turnover of the marine sponge Halisarca caerulea under steady-state conditions. The tropical coral reef sponge shows an extremely high proliferation activity, a short cell cycle duration and massive cell shedding. Cell turnover is predominantly confined to a single cell population, i.e. the choanocytes, and in this process apoptosis only plays a minor role. To our knowledge, such fast cell kinetics under steady-state conditions, with high turnover by shedding in the absence of apoptosis, has not been observed previously in any other multicellular organism. The duration of the cell cycle in vivo resembles that of unicellular organisms in culture. Morphological and histochemical studies demonstrate compartmentalization of choanocytes in the sponge tissue, which corresponds well with its remarkable cellular kinetics. Coral reef cavity sponges, like H. caerulea, inhabit low nutrient tropical waters, forcing these organisms to filter large volumes of water and to capture the few nutrients efficiently. Under these oligotrophic conditions, a high cell turnover may be considered as a very useful strategy, preventing permanent damage to the sponge by environmental stress. Halisarca caerulea maintains its body mass and keeps its food uptake system up to date by constantly renewing its filter system. We conclude that studies on cell kinetics and functional morphology provide new and essential information on the growth characteristics and the regulation of sponge growth in vivo as well as in vitro and the role of choanocytes in tissue homeostasis
Grazing, differential size-class dynamics and survival of the Mediterranean sponge Corticium candelabrum
Caralt, S. de; Uriz, M.J. ; Wijffels, R.H. - \ 2008
Marine Ecology Progress Series 360 (2008). - ISSN 0171-8630 - p. 97 - 106.
crambe-crambe poecilosclerida - coral-reef sponges - growth dynamics - population-structure - resource-allocation - mass-mortality - summer 1999 - deep-water - demospongiae - rates
The growth dynamics and survival of the sponge Corticium candelabrum (Demospongiae: Homosclerophorida) were surveyed in the northwestern Mediterranean for more than 3 yr. Growth and regeneration rates, fission and fusion events and survival were monitored monthly. Moreover, in situ punctual clearance experiments were conducted seasonally searching for possible relationships between food uptake and sponge dynamics. The monthly growth rates (GR) of C. candelabrum were low (0.19 ± 0.02 mean [±SE] for the 3 yr of study), variable and seasonal, with the highest values in summer. The cumulative survival function followed a stepped profile with several consecutive months without mortality separated by shorter mortality events, which mainly occurred in cold months (winter¿spring). However, an event of high mortality (76% of the monitored individuals died) took place in the particularly warm summer 2003. Fission events were frequent after previous damage (e.g. partial predation) and only one fusion event was recorded along the study period. The diet of C. candelabrum was highly heterogeneous. Differences in clearance rates (CR) among picoplankton types with season indicated that the sponge retained with different efficiency the several picoplankton types present in the water. Survival and GRs were significantly different for small, medium and large individuals (size-classes I, II and III), with the small sponges showing the lowest survival (56.6% cumulative mortality for the last 2 yr of study) and the highest GRs (0.18 ± 0.03 mo¿1, mean ± SE). On the whole, the results indicate that C. candelabrum is a slow-growing but dynamic sponge.
Cell culture from sponges: pluripotency and immortality
Caralt Bosch, S. de; Uriz, M.J. ; Wijffels, R.H. - \ 2007
Trends in Biotechnology 25 (2007)10. - ISSN 0167-7799 - p. 467 - 471.
stem-cell - hymeniacidon-perleve - suberites-domuncula - growth dynamics - in-vitro - marine - apoptosis - porifera - demospongiae - strategies
Sponges are a source of compounds with potential pharmaceutical applications. In this article, methods of sponge cell culture for production of these bioactive compounds are reviewed, and new approaches for overcoming the problem of metabolite supply are examined. The use of embryos is proposed as a new source of sponge material for cell culture. Stem cells are present in high amounts in embryos and are more versatile and resistant to infections than adult cells. Additionally, genetic engineering and cellular research on apoptotic mechanisms are promising new fields that might help to improve cell survival in sponge-cell lines. We propose that one topic for future research should be how to reduce apoptosis, which appears to be very high in sponge cell cultures.
Oxygen dynamics in choanosomal sponge explants
Hoffmann, F. ; Larsen, O. ; Rapp, H.T. ; Osinga, R. - \ 2005
Marine Biology Research 1 (2005)2. - ISSN 1745-1000 - p. 160 - 163.
marine sponges - chondrosia-reniformis - geodia-barretti - demospongiae - sediment - bacteria - ecology - culture - growth
Oxygen microprofiles were measured over the boundary layer and into the tissue of 10-day-old cultivated tissue fragments (explants of 2-4 cm 3) from the choanosome of the cold-water sponge Geodia barretti with oxygen-sensitive Clark-type microelectrodes. At this time of cultivation, the surface tissue and the aquiferous system of the explants is regenerating, which makes oxygen and nutrient supply by pumping activity impossible. Oxygen profiles showed a parabolic shape, indicating oxygen flux over a diffusive boundary layer and into the tissue. Oxygen was always depleted only 1 mm below the sponge surface, leaving the major part of the explants anoxic. Diffusive oxygen flux into the explant was calculated from three oxygen profiles using Fick's first law of diffusion and revealed 9 ¿mol O2 cm-3 day -1, which is in the lower range of in situ oxygen consumption of whole sponges. The ability of G. barretti to handle continuous tissue anoxia enables choanosomal explants to survive the critical first weeks of cultivation without a functional aquiferous system, when oxygen is supplied to the sponge explant by molecular diffusion over its surface.
Long-term culture of sponge explants: conditions enhancing survival and growth, and assessment of bioactivity
Caralt, S. de; Agell, G. ; Uriz, M.J. - \ 2003
Biomolecular Engineering 20 (2003)4-6. - ISSN 1389-0344 - p. 339 - 347.
crambe-crambe - suberites domuncula - marine sponges - dysidea-avara - demospongiae - primmorphs - poecilosclerida - aplysina - system
Sponges are an important source of secondary metabolites with pharmaceutical interest. This is the main reason for the increasing interest of sponge culture recent years. The optimal culture system depends on the species to be cultured: while some species easily produce sponge aggregates after dissociation (primmorphs), others show a great capacity to regenerate after fragmentation (explants). Corticium candelabrum is a Mediterranean bacteriosponge that can undergo asexual reproduction. We have taken advantage of this capability and cultured C. candelabrum explants under several experimental conditions. To find the best conditions for obtaining functional explants, we assayed a range of conditions, including seasons of collection, culture temperature, filtered versus filtered-sterile seawater, addition of antibiotics and proportion of ectosome. We monitored the changes in shape and ultrastructure during the formation of explants. After 24 h, TEM images showed the aquiferous system disarranged, in particular at the sponge periphery. From 2 to 4 weeks later, the aquiferous system regenerated, and fragments became functional sponges (explants). Explants were cultured under two regimes: in vitro and in a closed aquarium system. Antibiotics were only added to the in vitro culture to assess their effect on the symbiotic bacteria, which remained healthy despite the presence of antibiotics. Two food regimens (marine bacteria and green algae) were assayed for their ability to satisfy the metabolic requirements of explants. We monitored explant survival and growth. Explants showed a high long-term survival rate (close to 100%). Growth rates were higher in the closed aquarium system, without antibiotic addition, and fed with algae. Explants cultures were hardly contaminated because manipulation was reduced to a minimum and we used sterilized seawater. C. candelabrum produces bioactive molecules, which may play a defensive role in the sponge and may have pharmaceutical interest. The bioactivity of the explants was similar to that of wild sponges.
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