ATP distribution and localization of mitochondria in Suberites domuncula (Olivi 1792) tissue

Abstract

SUMMARYThe metabolic energy state of sponge tissue in vivo is largely unknown. Quantitative bioluminescence-based imaging was used to analyze the ATP distribution of Suberites domuncula (Olivi 1792) tissue, in relation to differences between the cortex and the medulla. This method provides a quantitative picture of the ATP distribution closely reflecting the in vivo situation. The obtained data suggest that the highest ATP content occurs around channels in the sponge medulla. HPLC reverse-phase C-18, used for measurement of ATP content, established a value of 1.62mol ATPg -1 dry mass in sponge medulla, as opposed to 0.04mol ATPg -1 dry mass in the cortex, thus indicating a specific and defined energy distribution. These results correlate with the mitochondria localization, determined using primary antibodies against cytochrome oxidase c subunit 1 (COX1) (immunostaining), as well as with the distribution of arginine kinase (AK), essential for cellular energy metabolism (in situ hybridization with AK from S. domuncula; SDAK), in sponge sections. The highest energy consumption seemed to occur in choanocytes, the cells that drive the water through the channel system of the sponge body. Taken together, these results showed that the majority of energetic metabolism in S. domuncula occurs in the medulla, in the proximity of aqueous channels.

Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter

“…Our NanoSIMS results offer one of the first insights into the fate of DOM after entering the sponge via the choanocytes. As mentioned above, part of the material may be directly metabolized by the choanocytes [10,55]. Our data show that metabolized products are then further processed reaching the dinoflagellate symbionts, implying that in C. orientalis, and potentially other phototrophic sponges, nutrients are to a certain extent cycled internally prior to being released.…”

“…This implies that vesicle-stored DOM was, at least partially, already processed within the first 3 h of our experiment, spreading the fixed material inside the choanocytes. The poor carbon signal in comparison may reflect preferential burning of carbon-rich compounds to fuel the energetically costly beating of choanocyte flagellae [10,55], or abovementioned methodological biases against carbon fixation in the sample processing [47].…”

Sponge bioerosion on changing reefs: ocean warming poses physiological constraints to the success of a photosymbiotic excavating sponge

“…Acidification similarly reduced uptake of DOC, which may point towards a trade-off between autotrophy (due to stimulation of photosynthesis under elevated p CO 2 ) and heterotrophy. Alternatively, prolonged high levels of H + may have had deleterious effects on the filter-feeding capacity of the sponge, for example by affecting mitochondrial ATP recycling which is crucial to the flagellar beating 80 . Further investigations are necessary to confirm what caused the observed decrease in carbon uptake under acidification.…”

Polyphosphate as a metabolic fuel in Metazoa: A foundational breakthrough invention for biomedical applications

“…In this context it is interesting to note that the high‐energy storage and liberating system via the arginine kinase evolved already in the most basal metazoans, the sponges (phylum Porifera) . More specific, the enzyme is localized in the mitochondria of those cells of these animals that show the highest energy consumption, the choanocytes, which represent the ‘motor’ cells in sponges . While under aerobic conditions the shuttling lipids show the highest rates of ATP production within the cells, they are the carbohydrates that meet this function under anaerobic conditions .…”