Elevated pCO₂ enhances under light but reduces in darkness the growth rate of a diatom, with implications for the fate of phytoplankton below the photic zone

Abstract

Experimentally elevated pCO2 and the associated pH drop are known to differentially affect many aspects of the physiology of diatoms under different environmental conditions or in different regions. However, contrasting responses to elevated pCO2 in the dark and light periods of a diel cycle have not been documented. By growing the model diatom Phaeodactylum tricornutum under 3 light levels and 2 different CO2 concentrations, we found that the elevated pCO2/pH drop projected for future ocean acidification reduced the diatom's growth rate by 8–25% during the night period but increased it by up to 9–21% in the light period, resulting in insignificant changes in growth over the diel cycle under the three different light levels. The elevated pCO2 increased the respiration rates irrespective of growth light levels and light or dark periods and enhanced its photosynthetic performance during daytime. With prolonged exposure to complete darkness, simulating the sinking process in the dark zones of the ocean, the growth rates decreased faster under elevated pCO2, along with a faster decline in quantum yield and cell size. Our results suggest that elevated pCO2 enhances the diatom's respiratory energy supplies to cope with acidic stress during the night period but enhances its death rate when the cells sink to dark regions of the oceans below the photic zone, with implications for a possible acidification‐induced reduction in vertical transport of organic carbon.

Ocean deoxygenation dampens resistance of diatoms to ocean acidification in darkness

“…On the contrary, decreased O 2 availability may benefit phytoplankton by slowing down the consumption of intracellular energy reserves. On the other hand, it is generally understood that the acidification associated with elevated pCO 2 increases the energy demands to drive H + extrusion (Taylor et al, 2012), which has been experimentally shown in diatoms (Wu et al, 2010;Goldman et al, 2017;Qu et al, 2021). Consequently, interactive effects of DeO 2 and acidification are expected, and we hypothesize that the resistance of diatoms to concurrent acid stress with increased pCO 2 may be affected by decreased pO 2 , since the availability of the latter impacts respiratory energy generation.…”

“…The reduced O 2 availability aided in such adjustment. On the other hand, elevated pCO 2 associated with the acidic stress is known to enhance respiration rate of diatoms to accommodate the increased energy demands involved in maintaining intracellular pH homeostasis (Wu et al, 2010;Goldman et al, 2017;Qu et al, 2021;Gao et al, 2022). However, a recent study suggests that the increased respiration may not be sufficient to counteract the negative effects induced by acidic stress in darkness, as the cell growth rate of the diatom P. tricornutum decreased in a 48-hour period of complete darkness (Qu et al, 2021).…”

“…On the other hand, elevated pCO 2 associated with the acidic stress is known to enhance respiration rate of diatoms to accommodate the increased energy demands involved in maintaining intracellular pH homeostasis (Wu et al, 2010;Goldman et al, 2017;Qu et al, 2021;Gao et al, 2022). However, a recent study suggests that the increased respiration may not be sufficient to counteract the negative effects induced by acidic stress in darkness, as the cell growth rate of the diatom P. tricornutum decreased in a 48-hour period of complete darkness (Qu et al, 2021). Thus, the diminished energy supply resulting from reduced O 2 availability may further weaken the ability of the diatoms to withstand acidic stress, leading to intensified biomass loss in T. pseudonana and delayed the recovery of both diatoms upon subsequent exposure to light in our experiment (Figure 1).…”

Deoxygenation enhances photosynthetic performance and increases N2 fixation in the marine cyanobacterium Trichodesmium under elevated pCO2

“…It is likely that the energy saved from downregulation of CMMs under HC was not enough to bring significant increase of net photosynthesis and growth rate ( Luo et al, 2019 ). Considering that phytoplankton can benefit from the elevated p CO 2 under light but suffer from the acidic stress in darkness, resulting in daytime enhanced and nighttime suppressed growth rates ( Qu et al, 2021 ), the net effects of the HC treatment on growth should be holistically considered for the diel cycle and availability of nutrients ( Table 2 ). We suggest that extra energy required to cope with the acidic stress under HC could be provided via increased dark respiration ( Figure 2 ), compensating for the insufficient energy supply from the downregulation of CCMs in Trichodesmium cells grown under HC.…”

High Light Intensity and CO2 Enrichment Synergistically Mitigated the Stress Caused by Low Salinity in Pyropia yezoensis

“…The effects of ocean acidification depend on the balance between the positive impact of increased CO 2 levels and the negative impact of reduced pH [22,46]. Moreover, the OA effect would also be influenced by other environmental stressors.…”