Forging sustainability

MigROS – The ‘behavioural photoprotection’ hypothesis revisited: coupling between vertical migration and photooxidative stress in estuarine microphytobenthos biofilms
Coordinator - João Serôdio
Programme - PTDC/MAR/112473/2009
Execution dates - 2011-03-01 - 2014-02-28 (36 Months)
Funding Entity - FCT
Funding for CESAM - 157908 €
Total Funding - 189204 €
Proponent Institution - Universidade de Aveiro
Participating Institutions
Fundação da Faculdade de Ciências
Université de La Rochelle
Netherlands Institute of Ecology

Marine biological productivity is largely based on the photosynthetic activity of diatoms, microalgae that account for 40% of global oceanic carbon fixation (1). In estuaries and shallow coastal zones, up to 50% of the ecosystem-level primary productivity is due to microphytobenthos (MPB), the diatom-dominated benthic communities that form dense biofilms on soft-sediment intertidal flats (2). The high photosynthetic performance of MPB under the extreme conditions of the intertidal habitat is considered to mostly rely upon highly efficient photoprotective processes that allow the cells to withstand direct exposure to solar irradiance during the prolonged periods of low tide (2,3). Exposure to high light causes photoinhibition, irreversible damages to the photosynthetic apparatus due to the accumulation of reactive oxygen species (ROS). Under the nutrient-replenished conditions of estuarine sediments, this photooxidative stress is expected to represent a major cause of limitation of photosynthetic productivity.

However, the understanding of the role of these processes in the success of MPB has been severely hampered by methodological difficulties regarding experimentation on intact biofilms (4). The source of these problems is simultaneously the most fascinating feature of these communities: a vertical migratory behaviour through which massive amounts of motile diatoms move within the uppermost layers of the sediment (5). The rapid migratory responses to changes in experimental conditions cause dramatic changes in biofilm biomass, species composition and physiological status that unavoidably confound the measurement of photophysiological parameters.

Due to the similar dimensions of the cells and of the sediment photic zone, benthic diatoms are presented with the exceptional situation of having the whole range of light intensities within their reach. This possibility lead to the formulation of the ‘behavioural photoprotection' hypothesis, according to which benthic diatoms adjust their position along the vertical light gradient as to optimize photosynthesis and minimize photodamages (6). This form of photoprotection would represent an energetically cheaper and more flexible mechanism than the physiological photoprotective processes shared with other photosynthetic organisms. It would be a key adaptation to the intertidal sedimentary environment that enables benthic diatoms to operate photosynthesis at so high levels. However, because of the impossibility of experimentally control cell migration while not disturbing biofilm structure and photosynthetic activity, this hypothesis has never been tested (7).

This project addresses the testing of the behavioural photoprotection hypothesis taking advantage of a recent methodological breakthrough that allows to obtain non-migratory but photosynthetically functional MPB biofilms. This method, developed by the PI and a team member, is based on the application of a diatom motility inhibitor to intact biofilms (8). This hypothesis will be tested in the broader context of the coupling between behavioural and physiological photoprotection against photooxidative stress in benthic diatoms.

The project will be developed through three main lines of research. Firstly, by testing the behavioural photoprotection hypothesis, by (a) confirming that the photobehaviour of benthic diatoms is related to photoinhibition susceptibility, and (b) quantifying the photoprotective role of vertical migration as compared to the effects of the main physiological processes. Photoinhibitory effects will be assessed by quantifying both the accumulation of ROS, the main harmful agents leading to photodamaging, as well as the effects of ROS action on the main cellular targets of photoinhibition.
Secondly, by testing the hypothesis that ROS act not only as harmful agents, but also as signalling molecules for photoprotective behaviour. This hypothesis is based on previous findings of the research team, and, if true, would represent the discovery of a new type of ROS-mediated intracellular signalling.
Thirdly, by investigating the existence of endogenously-controlled rhythmicity in the operation of physiological photoprotective processes. Benthic diatoms undergo strong endogenously-controlled vertical migratory rhythms closely synchronized with tidal and day/night cycles, and rhythms have been reported in the activation of photoprotective processes in other groups of microalgae. The finding of an endogenous coupling between vertical migration and physiological processes would establish the existence of a close link between behaviour and physiology of clear adaptive value to the intertidal environment.

The project's results will shed light on the interplay between photoprotection and oxidative stress in these unique photoautotrophic communities, and assess the role of photobehaviour in explaining the high productivity of estuarine intertidal areas.


Members on this project

PhD student
João Serôdio

Silja Frankenbach
Research Assistant

CESAM Funding: