Vertical cell movement is a primary response of intertidal benthic biofilms to increasing light dose

Abstract

Intertidal soft sediment microphytobenthic biofilms are often dominated by diatoms, which are able to regulate their photosynthesis by physiological processes (e.g. down-regulation through the xanthophyll cycle, referred to as non-photochemical quenching, NPQ) and behavioural processes (e.g. vertical cell movement in the sediment -biofilm matrix). This study investigated these 2 processes over a 6 h emersion period using chemical inhibitors under 2 light treatments (ambient and constant light at 300 µmol m -2 s -1). Latrunculin A (Lat A) was used to inhibit cell movement and dithiothreitol (DTT) to inhibit NPQ. HPLC analysis for chlorophyll a and spectral analysis (Normalised Difference Vegetation Index) indicated that Lat A significantly inhibited cell movement. Photosynthetic activity was measured using variable chlorophyll fluorescence and radiolabelled carbon uptake and showed that the non-migratory, Lat A-treated biofilms were severely inhibited as a result of the high accumulated light dose (significantly reduced maximum relative electron transport rate, rETR max , and light utilisation coefficient, α, compared to the migratory DTT and control-treated biofilms). No significant patterns were observed for 14 C data, although a decrease in uptake rate was observed over the measurement period. NPQ was investigated using HPLC analysis of xanthophyll pigments (diatoxanthin and the percentage de-epoxidation of diadinoxanthin), chlorophyll fluorescence (change in maximum fluorescence yield) and the 2nd order spectral derivative index (diatoxanthin index). Patterns between methods varied, but overall data indicated greater NPQ induction in the non-migratory Lat A treatment and little or no NPQ induction in the DTT and control treatments. Overall, the data resulted in 2 main conclusions: (1) the primary response to accumulated light dose was vertical movement, which when inhibited resulted in severe down-regulation/photoinhibition; (2) diatoms down-regulated their photosynthetic activity in response to accumulated light dose (e.g. over an emersion period) using a combination of vertical migration and physiological mechanisms that may contribute to diel and/or tidal patterns in productivity.KEY WORDS: Benthic · Diatom · Down-regulation · Migration · Photophysiology · ProductivityResale or republication not permitted without written consent of the publisher

Growth form defines physiological photoprotective capacity in intertidal benthic diatoms

“…EPL is not only more abundant in muddy cohesive sediments where light penetration is more restricted than in sandy sediments (Paterson and Hagerthey 2001;Cartaxana et al, 2011), but, more importantly, their (micro-) migratory behaviour allows positioning at the optimal irradiance in the vertical light gradient and rapid escape from periodic excess light (Kromkamp et al, 1998;Conn et al, 2004;Consalvey et al, 2004;Serô dio et al, 2006). This alleviates the need to invest in a strong physiological capacity to respond to light stress as previously proposed Cartaxana et al, 2011), although the right balance between motility and physiology still remains essential (van Leeuwe et al, 2009;Perkins et al, 2010b;Cartaxana et al, 2011;Serô dio et al, 2012). Such balance is more crucial in the EPM-M species, which can move but have only limited control over their immediate light environment as movement is restricted, usually within the sphere of individual sand grains.…”

“…To prevent photoinhibition (Serô dio et al, 2008), benthic diatoms utilize behavioural and physiological responses (Mouget et al, 2008;van Leeuwe et al, 2009;Perkins et al, 2010b;Cartaxana et al, 2011;Serôdio et al, 2012). Behavioural photoprotection involves motility, allowing cells to position themselves in light gradients and escape from prolonged exposure to excess light (Admiraal, 1984;Kromkamp et al, 1998;Consalvey et al, 2004;Serô dio et al, 2006).…”

Spatio-temporal variability in Mediterranean rocky shore microphytobenthos

“…In intertidal soft sediments, microphytobenthos (generally diatom dominated) exhibit rhythmic vertical migrations across the photic zone of the sediment, related to tidal and day−night cycles, usually moving downwards at high tide to intercept light and/or escape grazers and predators (Consalvey et al 2004). In addition, at low tide under supersaturating light intensities, diatoms exhibit a negative phototaxis resulting in downward micro-migration (Perkins et al 2010). From a physiological perspective, both diatoms and cyanobacteria can dissipate excess energy through non-photochemical quenching (NPQ) of chl a fluorescence (Bailey & Grossman 2008, Perkins et al 2010, as well as synthesize EPS substances, which are typically produced during emersion periods to protect them against desiccation and facilitate movement (Decho 1990, Potts 1999, Underwood & Paterson 2003.…”

“…In addition, at low tide under supersaturating light intensities, diatoms exhibit a negative phototaxis resulting in downward micro-migration (Perkins et al 2010). From a physiological perspective, both diatoms and cyanobacteria can dissipate excess energy through non-photochemical quenching (NPQ) of chl a fluorescence (Bailey & Grossman 2008, Perkins et al 2010, as well as synthesize EPS substances, which are typically produced during emersion periods to protect them against desiccation and facilitate movement (Decho 1990, Potts 1999, Underwood & Paterson 2003. What can observed changes in RVI on a daily scale tell us about physiological and behavioral responses of rocky shore EMPB to increasing irradiance or desiccation conditions?…”

Evidence for gravitactic behaviour in benthic diatoms

“…Recently, vertical migration has been investigated and recognized as a photoprotective mechanism, operating complementarily to the main physiological photoprotection processes (e.g. the xanthophyll cycle; Mouget et al, 2008;Serôdio et al, 2008Serôdio et al, , 2012Perkins et al, 2010;Cartaxana et al, 2011).…”