Redox state, reactive oxygen species and adaptive growth in colonial hydroids

Colonial metazoans often encrust surfaces over which the food supply varies in time or space. In such an environment, adaptive colony development enta ils adjusting the timing and spacing of feeding structures and gastrovascul ar connections to correspond to this variable food supply. To investigate t he possibility of such adaptive growth, within-colony differential feeding experiments were carried out using the hydroid Podocoryna carnea, Indeed, s uch colonies strongly exhibited adaptive growth, developing dense arrays of polyps (feeding structures) and gastrovascular connections in areas that w ere fed relative to areas that were starved, and this effect became more co nsistent over time. To investigate mechanisms of signaling between the food supply and colony development, measurements were taken of metabolic parame ters that have been implicated in signal transduction in other systems, par ticularly redox state and levels of reactive oxygen species. Utilizing fluo rescence microscopy of P, carnea cells in vivo, simultaneous measurements o f redox state [using NAD(P)H] and hydrogen peroxide (using 2 ' ,7 ' -dichio rofluorescin diacetate) were taken. Both measures focused on polyp epitheli omuscular cells, since these exhibit the greatest metabolic activity. Colon ies 3-5 h after feeding were relatively oxidized, with low levels of peroxi de, while colonies 24h after feeding were relatively reduced, with high lev els of peroxide. The functional role of polyps in feeding and generating ga strovascular flow probably produced this dichotomy, Polyps 3-5h after feedi ng contract maximally, and this metabolic demand probably shifts the redox state in the direction of oxidation and diminishes levels of reactive oxyge n species. In contrast, 24h after feeding, polyps are quiescent, and this l ack of metabolic demand probably shifts the redox state in the direction of reduction and increases levels of reactive oxygen species. Within-colony d ifferential feeding experiments were carried out on colonies 24h after the usual, colony-wide feeding. At this time, a single polyp was fed, and this polyp was compared with an otherwise similar polyp from the same colony. A pattern similar to the whole-colony experiments was obtained: the just-fed polyp, as it begins contracting shortly after feeding, appears to be relati vely oxidized, with low levels of peroxide compared with the polyp that was not fed. These data are consistent with the hypothesis that adaptive colon y development in response to a variable food supply is mediated by redox st ate or reactive oxygen species or both, although alternative hypotheses are also discussed.