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The upside-down jellyfish, Cassiopea spp., host their algal symbionts inside a subset of amoebocytes, phagocytic cells that also play innate immune functions akin to macrophages from vertebrate animals. Amoebocyte precursors phagocytose algae from the jellyfish gut and store them inside intracellular compartments called symbiosomes. Subsequently, the precursors migrate to the mesoglea, differentiate into symbiotic amoebocytes, and roam throughout the jellyfish body where the algae remain photosynthetically active and supply the jellyfish host with a significant portion of their organic carbon needs. Here, we show that the amoebocyte symbiosome membrane contains V-H+-ATPase (VHA), the proton pump that acidifies phagosomes and lysosomes in all eukaryotes. Many symbiotic amoebocytes also abundantly express a carbonic anhydrase (CA), an enzyme that reversibly hydrates CO2 into H+ and HCO3−. Moreover, we found that the symbiosome lumen is pronouncedly acidic and that pharmacological inhibition of VHA or CA activities significantly decreases photosynthetic oxygen production in live jellyfish. These results point to a carbon concentrating mechanism (CCM) that co-opts VHA and CA from the phago-lysosomal machinery that ubiquitously mediates food digestion and innate immune responses. Analogous VHA-dependent CCMs have been previously described in reef-building corals, anemones, and giant clams; however, these other two cnidarians host their dinoflagellate algae inside gastrodermal cells -not in amoebocytes- and the clam hosts theirs within the gut lumen. Thus, our study identifies an example of convergent evolution at the cellular level that might broadly apply to invertebrate-microbe photosymbioses while also providing evolutionary links with intra- and extracellular food digestion and the immune system. 

ABSTRACT The regulation of ionic, osmotic and acid–base (IOAB) conditions in biological fluids is among the most fundamental functions in all organisms; being surrounded by water uniquely shapes the IOAB regulatory strategies of water-breathing animals. Throughout its centennial history, Journal of Experimental Biology has established itself as a premier venue for publication of comparative, environmental and evolutionary studies on IOAB regulation. This Review provides a synopsis of IOAB regulation in aquatic animals, some of the most significant research milestones in the field, and evolving views about the underlying cellular mechanisms and their evolutionary implications. It also identifies promising areas for future research and proposes ideas for enhancing the impact of aquatic IOAB research. 

Biomineralizing cells concentrate dissolved inorganic carbon (DIC) and remove protons from the site of mineral precipitation. However, the molecular regulatory mechanisms that orchestrate pH homeostasis and biomineralization of calcifying cells are poorly understood. Here, we report that the acid-base sensing enzyme soluble adenylyl cyclase (sAC) coordinates intracellular pH (pH i ) regulation in the calcifying primary mesenchyme cells (PMCs) of sea urchin larvae. Single-cell transcriptomics, in situ hybridization, and immunocytochemistry elucidated the spatiotemporal expression of sAC during skeletogenesis. Live pH i imaging of PMCs revealed that the downregulation of sAC activity with two structurally unrelated small molecules inhibited pH i regulation of PMCs, an effect that was rescued by the addition of cell-permeable cAMP. Pharmacological sAC inhibition also significantly reduced normal spicule growth and spicule regeneration, establishing a link between PMC pH i regulation and biomineralization. Finally, increased expression of sAC mRNA was detected during skeleton remineralization and exposure to CO 2 -induced acidification. These findings suggest that transcriptional regulation of sAC is required to promote remineralization and to compensate for acidic stress. This work highlights the central role of sAC in coordinating acid-base regulation and biomineralization in calcifying cells of a marine animal. 

White seabass ( Atractoscion nobilis) increasingly experience periods of low oxygen (O 2 ; hypoxia) and high carbon dioxide (CO 2 , hypercapnia) due to climate change and eutrophication of the coastal waters of California. Hemoglobin (Hb) is the principal O 2 carrier in the blood and in many teleost fishes Hb-O 2 binding is compromised at low pH; however, the red blood cells (RBC) of some species regulate intracellular pH with adrenergically stimulated sodium-proton-exchangers (β-NHEs). We hypothesized that RBC β-NHEs in white seabass are an important mechanism that can protect the blood O 2 -carrying capacity during hypoxia and hypercapnia. We determined the O 2 -binding characteristics of white seabass blood, the cellular and subcellular response of RBCs to adrenergic stimulation, and quantified the protective effect of β-NHE activity on Hb-O 2 saturation. White seabass had typical teleost Hb characteristics, with a moderate O 2 affinity (Po 2 at half-saturation; P 50 2.9 kPa) that was highly pH-sensitive (Bohr coefficient −0.92; Root effect 52%). Novel findings from super-resolution microscopy revealed β-NHE protein in vesicle-like structures and its translocation into the membrane after adrenergic stimulation. Microscopy data were corroborated by molecular and phylogenetic results and a functional characterization of β-NHE activity. The activation of RBC β-NHEs increased Hb-O 2 saturation by ∼8% in normoxic hypercapnia and by up to ∼20% in hypoxic normocapnia. Our results provide novel insight into the cellular mechanism of adrenergic RBC stimulation within an ecologically relevant context. β-NHE activity in white seabass has great potential to protect arterial O 2 transport during hypoxia and hypercapnia but is less effective during combinations of these stressors.