Morphological, Genetic, and Physiological Effects of Nutrient Manipulation on a Colonial Marine Hydroid.

AbstractThe availability of environmental nutrients is an existential constraint for heterotrophic organisms and is thus expected to impact numerous biochemical and physiological features. The continuously proliferative polyp stage of colonial hydroids provides a useful model to study these features, allowing genetically identical replicates to be compared. Two groups of colonies of Eirene sp., defined by different feeding treatments, were grown by explanting the same founder colony onto cover glass. Colonies of both treatments were allowed to grow continuously by explanting them onto new cover glass as they reached the edge of the existing surface. The nutrient-abundant polyps grew faster and produced more clumped or "sheet-like" colonies. Compared to the founder colony, the nutrient-abundant colonies exhibited more mutations (i.e., single-nucleotide polymorphisms) than the nutrient-scarce colonies. Nevertheless, these differences were not commensurate with the differences in growth. Using a polarographic electrode, we found that the nutrient-abundant colonies exhibited lower rates of oxygen uptake relative to total protein. The probe 2',7'-dichlorodihydrofluorescein diacetate and fluorescent microscopy allowed visualization of the mitochondrion-rich cells at the base of the polyps and showed that the nutrient-abundant colonies exhibited greater amounts of reactive oxygen species than the nutrient-scarce colonies. Parallels to the Warburg effect-aerobic glycolysis, diminished oxygen uptake, and lactate secretion-found in human cancers and other proliferative cells may be suggested. However, little is known about anaerobic metabolism in cnidarians. Examination of oxygen uptake suggests an anaerobic threshold at a roughly 1-mg/L oxygen concentration. Nutrient-abundant colonies may respond more dramatically to this threshold than nutrient-scarce colonies.

An Organismal Perspective on the Warburg Effect and Models for Proliferation Studies.

Interest in the physiology of proliferation has been generated by human proliferative diseases, i.e., cancers. A vast literature exists on the Warburg effect, which is characterized by aerobic glycolysis, diminished oxygen uptake, and lactate secretion. While these features could be rationalized via the production of biosynthetic precursors, lactate secretion does not fit this paradigm, as it wastes precursors. Forming lactate from pyruvate allows for reoxidizing cytosolic NADH, which is crucial for continued glycolysis and may allow for maintaining large pools of metabolic intermediates. Alternatively, lactate production may not be adaptive, but rather reflect metabolic constraints. A broader sampling of the physiology of proliferation, particularly in organisms that could reoxidize NADH using other pathways, may be necessary to understand the Warburg effect. The best-studied metazoans (e.g., worms, flies, and mice) may not be suitable, as they undergo limited proliferation before initiating meiosis. In contrast, some metazoans (e.g., colonial marine hydrozoans) exhibit a stage in the life cycle (the polyp stage) that only undergoes mitotic proliferation and never carries out meiosis (the medusa stage performs this). Such organisms are prime candidates for general studies of proliferation in multicellular organisms and could at least complement the short-generation models of modern biology.