Migration or photoacclimation to prevent high irradiance and UV-B damage in marine microphytobenthic communities

Abstract

Microphytobenthos (MPB) on intertidal mudflats is a major component of primary producers in some estuarine ecosystems. To sustain photosynthesis, MPB migrate through the upper sediment layer and form transient biofilms during emersion periods, and thus may be exposed to high irradiance and ultraviolet radiation (UV-R), possibly resulting in photodamage to the photosynthetic apparatus. In contrast, downard migration could allow cells to optimize position in the photic zone, avoiding photoinhibitory light levels. Engineered biofilms with inhibited migratory capacity were used to distinguish between possible strategies (photoacclimation or migration) evolved by MPB to cope with photoinhibitory irradiances, when a series of UV filters with different cut-off wavelengths was used to estimate the respective contribution of visible light and UV-R. Engineered biofilms with full migratory capacity maintained a high relative electron transport rate (rETR), in contrast to engineered non-migratory biofilms, which showed a decrease in rETR under high irradiance, with a greater decrease under UV-B radiation. Migration thus appeared to be the principal short-term mechanism allowing MPB to avoid or minimize UV-R and high PAR photodamage in situ. Nevertheless, physiological acclimation processes to different light levels ('light-shade' patterns) seem to occur in the long term, and probably superimpose on migratory capacity, making light history an important component of MPB photoacclimation strategies. KEY WORDS: Microphytobenthos · Migration · Photodamage · Photoinhibition · Ultraviolet radiation Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 52: [223][224][225][226][227][228][229][230][231][232] 2008 benthic algae show complex patterns of vertical migration within sediments, further complicated by variations in light environment and other environmental variables (temperature, salinity, nutrient and water availability, alternation of seasons). Moreover, water currents and meteorological events can disturb biofilm structure and dynamics. MPB photosynthesis is limited to the emersion periods, and daytime emersion can occur once (around midday) or twice a day (morning and afternoon), as a function of tidal and nycthemeral rhythms. MPB can thus be exposed to irradiances up to, and sometimes in excess of, 2000 µmol m -2 s -1 , when emersion coincides with midday maxima in irradiance (Underwood & Kromkamp 1999, Perkins et al. 2001). At such high irradiance, planktonic microalgae usually show a decrease in photosynthesis, the extent of which varies according to irradiance level, time or length of exposure, and light history (the accumulated light dose to which the cells have been exposed previously). The decrease in photosynthetic activity caused by high irradiances can be attributed to different phenomena (photoprotection, photoinactivation, photoinhibition, photoacclimation), depending on the time scale considered, the possible existence of photodamage to the components of...

Effect of light on photosynthetic efficiency of sequestered chloroplasts in intertidal benthic foraminifera (<i>Haynesina germanica</i> and <i>Ammonia tepida</i>)

“…Not only will they have easy access to fresh diatom chloroplasts, as H. germanica is mainly living in the first few millimetres of the superficial sediment (Alve and Murray, 2001;Thibault de Chanvalon et al, 2015), but they will also have the possibility of migrating within the sediment (Gross, 2000) using this behavioural feature to enhance their photoregulation capacity, similar to what is observed in benthic diatoms from microphytobenthic biofilms (e.g. Jesus et al, 2006;Mouget et al, 2008;Perkins et al, 2010). However, below the photic limit (max 2 to 3 mm in estuarine sediments reviewed in MacIntyre et al, 1996;Cartaxana et al, 2011) it is unlikely that oxygenic photosynthesis will occur, even if live H. german-…”

Efficiency of photoprotection in microphytobenthos: role of vertical migration and the xanthophyll cycle against photoinhibition

“…This subject has attracted substantial attention in recent years, particularly centered on the effects of vertical migration on biofilm photophysiology (Consalvey et al 2004, Jesus et al 2006, Waring et al 2007, Mouget et al 2008, Perkins et al 2010, Cartaxana et al 2011, and has been facilitated by the introduction of a diatom motility inhibitor (Cartaxana et al. 2008).…”

“…In contrast, the negative phototactic be havior of benthic dia toms, mostly raphid pennates, under high light has long been interpreted as a form of avoidance of excessive light levels that would otherwise cause photoinhibition (Admiraal 1984, Consalvey et al 2004, Waring et al 2007). This subject has attracted substantial attention in recent years, particularly centered on the effects of vertical migration on biofilm photophysiology (Consalvey et al 2004, Jesus et al 2006, Waring et al 2007, Mouget et al 2008, Perkins et al 2010, Cartaxana et al 2011, and has been facilitated by the introduction of a diatom motility inhibitor (Cartaxana et al. 2008).…”

“…However, although some studies have shown a relation between migratory cell size and migratory behavior in sediments (Hay et al 1993, Underwood et al 2005, there is no evidence that cell size is an important factor regarding the migratory response to light stress. Also, the selective nature of the sampling method used may have resulted in an underestimation of the true variability in species composition at the surface.Vertical migration and the xanthophyll cycle have been considered as the main photoprotective mechanisms in microphytobenthic biofilms (Serôdio et al 2005, Jesus et al 2006, Mouget et al 2008, Perkins et al 2010. A perhaps surprising result of the present study is the relatively low contribution of these 2 processes to overall photoprotection.…”

Growth form defines physiological photoprotective capacity in intertidal benthic diatoms

“…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).…”