The Influence of Symbiosis on the Proteome of the Exaiptasia Endosymbiont Breviolum minutum.

The cellular mechanisms responsible for the regulation of nutrient exchange, immune response, and symbiont population growth in the cnidarian-dinoflagellate symbiosis are poorly resolved. Here, we employed liquid chromatography-mass spectrometry to elucidate proteomic changes associated with symbiosis in Breviolum minutum, a native symbiont of the sea anemone Exaiptasia diaphana ('Aiptasia'). We manipulated nutrients available to the algae in culture and to the holobiont in hospite (i.e., in symbiosis) and then monitored the impacts of our treatments on host-endosymbiont interactions. Both the symbiotic and nutritional states had significant impacts on the B. minutum proteome. B. minutum in hospite showed an increased abundance of proteins involved in phosphoinositol metabolism (e.g., glycerophosphoinositol permease 1 and phosphatidylinositol phosphatase) relative to the free-living alga, potentially reflecting inter-partner signalling that promotes the stability of the symbiosis. Proteins potentially involved in concentrating and fixing inorganic carbon (e.g., carbonic anhydrase, V-type ATPase) and in the assimilation of nitrogen (e.g., glutamine synthase) were more abundant in free-living B. minutum than in hospite, possibly due to host-facilitated access to inorganic carbon and nitrogen limitation by the host when in hospite. Photosystem proteins increased in abundance at high nutrient levels irrespective of the symbiotic state, as did proteins involved in antioxidant defences (e.g., superoxide dismutase, glutathione s-transferase). Proteins involved in iron metabolism were also affected by the nutritional state, with an increased iron demand and uptake under low nutrient treatments. These results detail the changes in symbiont physiology in response to the host microenvironment and nutrient availability and indicate potential symbiont-driven mechanisms that regulate the cnidarian-dinoflagellate symbiosis.

Increased cellular detoxification, cytoskeletal activities and protein transport explain physiological stress in a lagoon sponge.

Tropical lagoon-inhabiting organisms live in highly irradiated ecosystems and are particularly susceptible to thermal stress resulting from climate change. However, despite living close to their thermal maxima, stress response mechanisms found in these organisms are poorly understood. We used a novel physiological-proteomic approach for sponges to describe the stress response mechanisms of the lagoon-inhabiting sponge Amphimedon navalis, when exposed to elevated seawater temperatures of +2°C and +4°C relative to a 26°C ambient temperature for 4 weeks. After 4 weeks of thermal exposure, the buoyant weight of the sponge experienced a significant decline, while its pumping rates and oxygen consumption rates significantly increased. Proteome dynamics revealed 50 differentially abundant proteins in sponges exposed to elevated temperature, suggesting that shifts in the sponge proteome were potential drivers of physiological dysfunction. Thermal stress promoted an increase in detoxification proteins, such as catalase, suggesting that an excess of reactive oxygen species in sponge cells was responsible for the significant increase in oxygen consumption. Elevated temperature also disrupted cellular growth and cell proliferation, promoting the loss of sponge biomass, and the high abundance of multiple α-tubulin chain proteins also indicated an increase in cytoskeletal activities within sponge cells, which may have induced the increase in sponge pumping rate. Our results show that sustained thermal exposure in susceptible lagoonal sponges may induce significant disruption of cellular homeostasis, leading to physiological dysfunction, and that a combined physiological-proteomic approach may provide new insights into physiological functions and cellular processes occurring in sponges.

Interocean patterns in shallow water sponge assemblage structure and function.

Sponges are a major component of benthic ecosystems across the world and fulfil a number of important functional roles. However, despite their importance, there have been few attempts to compare sponge assemblage structure and ecological functions across large spatial scales. In this review, we examine commonalities and differences between shallow water (<100 m) sponges at bioregional (15 bioregions) and macroregional (tropical, Mediterranean, temperate, and polar) scales, to provide a more comprehensive understanding of sponge ecology. Patterns of sponge abundance (based on density and area occupied) were highly variable, with an average benthic cover between ~1 and 30%. Sponges were generally found to occupy more space (percentage cover) in the Mediterranean and polar macroregions, compared to temperate and tropical macroregions, although sponge densities (sponges m-2 ) were highest in temperate bioregions. Mean species richness standardised by sampling area was similar across all bioregions, except for a few locations that supported very high small-scale biodiversity concentrations. Encrusting growth forms were generally the dominant sponge morphology, with the exception of the Tropical West Atlantic, where upright forms dominated. Annelids and Arthropods were the most commonly reported macrofauna associated with sponges across bioregions. With respect to reproduction, there were no patterns in gametic development (hermaphroditism versus gonochorism), although temperate, tropical, and polar macroregions had an increasingly higher percentage of viviparous species, respectively, with viviparity being the sole gamete development mechanism reported for polar sponges to date. Seasonal reproductive timing was the most common in all bioregions, but continuous timing was more common in the Mediterranean and tropical bioregions compared to polar and temperate bioregions. We found little variation across bioregions in larval size, and the dominant larval type across the globe was parenchymella. No pattens among bioregions were found in the limited information available for standardised respiration and pumping rates. Many organisms were found to predate sponges, with the abundance of sponge predators being higher in tropical systems. While there is some evidence to support a higher overall proportion of phototrophic species in the Tropical Austalian bioregion compared to the Western Atlantic, both also have large numbers of heterotrophic species. Sponges are important spatial competitors across all bioregions, most commonly being reported to interact with anthozoans and algae. Even though the available information was limited for many bioregions, our analyses demonstrate some differences in sponge traits and functions among bioregions, and among macroregions. However, we also identified similarities in sponge assemblage structure and function at global scales, likely reflecting a combination of regional- and local-scale biological and physical processes affecting sponge assemblages, along with common ancestry. Finally, we used our analyses to highlight geographic bias in past sponge research, and identify gaps in our understanding of sponge ecology globally. By so doing, we identified key areas for future research on sponge ecology. We hope that our study will help sponge researchers to consider bioregion-specific features of sponge assemblages and key sponge-mediated ecological processes from a global perspective.

Short-term responses of tropical lagoon sponges to elevated temperature and nitrate.

Sponges are often important components of coastal lagoons, however their responses to anthropogenic stressors remain poorly understood. Here, we tested the responses of three lagoon sponges, Neopetrosia exigua, Amphimedon navalis and Spheciospongia vagabunda from Mauritius (Western Indian Ocean), to nine temperature and nitrate combinations for 14 days. We found that elevated seawater temperature resulted in significant physiological responses in all species, but there was generally little negative effect of elevated nitrate. At the end of the experiment, the buoyant weight of all three species were significantly reduced, while for the two chlorophyll a-containing species, N. exigua and S. vagabunda, effective quantum yield (ΔF/Fm') of photosystem (PS) II, photosynthetic pigment concentrations, gross photosynthetic rate and gross photosynthesis to respiration (P:R) ratio were also reduced. Dark respiration rates were higher in all three species at elevated temperature. While these lagoon sponges appeared to be impacted by elevated temperature, here, we demonstrate that these species are physiologically tolerant to excess nitrate concentrations.