Redox control in development and evolution: evidence from colonial hydroids

Abstract

Redox chemistry, involving the transfer of electrons and hydrogen atoms, is central to energy conversion in respiration, and the control of gene expression by redox state commonly occurs in bacteria, allowing rapid responses to environmental changes, for instance, in the food supply. Colonial metazoans often encrust surfaces over which the food supply varies in time or space; hence, in these organisms, redox control of the development of feeding structures and gastrovascular connections could be similarly adaptive, allowing colonies to adjust the timing and spacing of structures in response to a variable food supply. To investigate the possibility of redox control of colony development, the redox states of hydractiniid hydroid colonies were manipulated experimentally. As in many colonial animals, hydractiniid hydroids display a range of morphological variation from sheet-like forms (i.e. closely spaced polyps with high rates of stolon branching) to runner-like forms (i. e. widely spaced polyps with low rates of stolon branching). In the runner-like Podocoryna carnea, azide, a blocker of the electron transport chain, and dinitrophenol, an uncoupler of oxidative phosphorylation, diminished the largely polyp-driven gastrovascular flow to a similar extent. Measures of the redox state of the polyp epitheliomuscular cells using the fluorescence of NAD(P)H suggest that azide shifts the redox state in the direction of reduction, while dinitrophenol shifts the redox state in the direction of oxidation. Colony development corresponds to redox state in that azide-treated colonies were more runner-like, while dinitrophenol-treated colonies were more sheet-like. Nevertheless, the functional role of polyps in feeding and generating gastrovascular flow probably contributed to a trade-off between polyp number and size such that azide-treated colonies had few large polyps, while dinitrophenol-treated colonies had many small polyps. Regardless of the treatment, P. carnea colonies developed to maturity and produced swimming medusae in the normal fashion. In the sheet-like Hydractinia symbiolongicarpus, treatment with azide resulted in complete suppression of the development of both the stolonal mat and the blastostyles, the reproductive polyps. Azide-treated H. symbiolongicarpus colonies therefore developed in a juvenilized, runner-like manner and much resembled colonies of P. carnea. Following cessation of azide treatment in H. symbiolongicarpus, normal colony development ensued, and both a stolonal mat and blastostyles formed. In both hydroid species, relative oxidization favors sheet-like growth, while relative reduction favors runner-like growth. Since feeding triggers strong contractions of polyp epitheliomuscular cells and results in relative oxidation, this experimental evidence supports the hypothesis of adaptive redox control of colony development and evolution.