Taxon‐specific dark survival of diatoms and flagellates affects Arctic phytoplankton composition during the polar night and early spring

Abstract

Effects of prolonged darkness on Arctic phytoplankton composition were investigated with lab experiments and a pigment time series in Kongsfjorden, Spitsbergen (78 55 0 N). Chlorophyll a (Chl a), pigment composition, particulate organic carbon, cell numbers, and photosynthetic characteristics were studied in Arctic diatoms (Thalassiosira antarctica, Thalassiosira nordenskioeldii) and flagellates (Rhodomonas sp., Micromonas sp.) during 8 weeks of darkness and subsequent recovery in irradiance. Loss of photosynthetic functionality after 2 weeks of darkness was reversible in all species when returned to irradiance. Diatoms were more resistant to prolonged darkness (> 2 weeks) compared to the flagellates, with lower decline rates of Chl a and maximum quantum yield of PSII. T. nordenskioeldii showed rapid growth during recovery throughout 8 weeks of dark incubation, whereas recovery of flagellates diminished within 4 weeks. Ratios of taxonomic marker pigments relative to Chl a of all species showed limited variation during 8 weeks of dark incubation. The experimentally observed enhanced dark survival of diatoms was in agreement with pigment observations during four polar nights (2013)(2014)(2015)(2016)(2017) in Kongsfjorden, which showed increased relative diatom abundance during declining biomass (down to 0.02 mg Chl a m −3 ). Therefore, a period of prolonged darkness gives Arctic diatoms a head start during the early stages of the spring bloom. The taxon-specific survival traits can influence the geographical distribution of diatoms and flagellates within the polar oceans and their phenology. Furthermore, the persistence of Chl a of nonviable phytoplankton during darkness might influence biomass estimates during the polar night.

Solar radiation and solar radiation driven cycles in warming and freshwater discharge control seasonal and inter‐annual phytoplankton chlorophyll a and taxonomic composition in a high Arctic fjord (Kongsfjorden, Spitsbergen)

“…Indeed, flagellated phytoplankton pigments declined during autumn and winter, causing a pronounced increase in diatom relative abundance. This suggests survival of diatoms during prolonged darkness, which is in agreement with dark survival experiments with diatoms and flagellates (Smayda and Mitchell‐Innes 1974, van de van de Poll et al 2019). Apart from reducing phytoplankton irradiance exposure, the expanding mixed layer can also entrain diatoms from deeper water layers and the ocean floor.…”

“…Moreover, diatom relative abundance was in good agreement with independent observations of silicic acid concentrations. Previous research indicated that ratios of fucoxanthin and other marker pigments of diatoms and flagellates relative to Chl a were stable during 8 weeks of darkness (i.e., pigments declined equally, van de Poll et al 2019). Pigments and CHEMTAX based phytoplankton composition provide coarse information, with no resolution beyond the taxonomic level.…”

Rapid photoacclimation during episodic deep mixing augments the biological carbon pump

“…Diatoms are known for their efficient growth under low light and rapid responses to increasing light availability (Geider et al 1986; Fisher and Halsey 2016; Poll et al 2019). In our experiments, photoacclimation of the diatom T. pseudonana outpaced the green alga, D. tertiolecta , following the shift from high to low light.…”

“…Most research on photoacclimation has examined phytoplankton physiology under balanced growth (Laws and Bannister 1980; Fisher and Halsey 2016) or in response to rapid increases in light to understand mechanisms involved in photoprotection of photosynthetic reaction centers (Lavaud et al 2004; Zhu and Green 2010). On timescales ranging from seconds to hours, diatoms decrease NPQ and alter carbon allocation mechanisms to sustain growth under decreasing light and even after exposure to darkness (Lohr and Wilhelm 1999; Bailleul et al 2010; Poll et al 2019). Green algae also decrease NPQ capacity, and their growth rate can slow drastically following a shift from high light to low light conditions (LaRoche et al 1991).…”

Linking extreme seasonality and gene expression in arctic marine protists

“…This includes crucial primary producers, such as Micromonas polaris, which were encountered as active at different depths of Arctic marine habitats during polar night [14]. Persistence of low levels of light-dependent biological processes in primary producers during polar night is likely due to the persistence and perhaps even maintenance of a functional photosynthetic apparatus kept ready to be activated once the light comes back [13], [30]. Therefore an overrepresentation of eukaryotic proteorhodopsins during polar night was rather unexpected, as bacterial proteorhodopsins are known to contribute to an alternative pathway to photosynthesis being the main contributors to harnessing solar energy in the ocean [82].…”