When ocean deoxygenation meets phytoplankton

Reduced oxygen increased primary productivity of a coastal phytoplankton assemblage and enhanced photosynthesis and growth in cultures of a coastal diatom, suggesting that phytoplankton photosynthesis could enhance re-oxygenation processes in hypoxic areas.

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Hypoxic waters, defined as having dissolved O2 < 63 μM, occur naturally in either open ocean or nearshore waters. Reduced vertical exchange of oxygen and the enhanced biological remineralization due to anthropogenic global warming and eutrophication have enhanced the spatial extent and severity of hypoxic zones, especially in coastal regions, resulting in extremely low O2, low pH, and high CO2 conditions, and degraded habitat fitness for aerobic marine organisms. Although hypoxia is usually associated with deep water environments, near-surface hypoxic waters (< 20 m) are often observed in coastal regions due to extreme deoxygenation processes and upwelling currents and can be maintained even for several weeks. However, until recently there has been little work examining the impacts of lowered oxygen levels on photosynthesis of the phytoplankton, the main primary producers and drivers of marine food chains.

In June 2015, we participated in a research cruise examining primary production in the Pearl River estuary and decided to take advantage of this opportunity to explore the relationship between dissolved oxygen (DO) and photosynthesis in situ. Excitingly, after excluding effects of other environmental factors, data showed a significant correlation of higher photosynthetic light use efficiency (PLUE) with lower dissolved oxygen (DO), which suggested that DO could be one of the key drivers influencing in situ photosynthesis and primary production - something that has seldom been considered previously. This has the corollary that enhanced photosynthesis under low DO would lead to increased O2 production by phytoplankton, thereby ameliorating the extent of hypoxia.

Accordingly, we followed this up by conducting a 30 litre mesocosm experiment outdoors at the Dongshan Swire Station of Xiamen University to test the responses of a natural coastal phytoplankton assemblage to different combinations of DO and CO2, chosen to mimic effects of hypoxia and elevated CO2 associated with global change. During the mesocosm experiment, the net and gross photosynthetic rates were higher in low O2 systems at both ambient and elevated CO2 levels than they were under ambient O2 levels. Furthermore, the photochemical yield (reflecting the efficiency of photosynthetic light energy conversion) and effective functional absorption cross-section (an indicator of the efficiency of light capture) were both higher in phytoplankton assemblages grown under low O2while a process termed non-photochemical quenching (an indicator of photosynthetic energy loss as heat dissipation and a signal of light stress) was lower, regardless of CO2 levels. These results thus backed up the cruise data suggesting enhanced photosynthesis and photosynthetic energy transfer in low O2-grown phytoplankton.

The central enzyme of photosynthesis, ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), possesses both carboxylation and oxygenation activities to fix CO2 and to consume O2, respectively, which act competitively with one another, the oxygenase reaction leading to photorespiration and CO2 loss. The expansion of hypoxic waters may thus alter the catalytic direction of the enzyme by decreasing the ratio of O2 to CO2, favoring the carboxylase activity and thereby promoting photosynthesis.

Diatoms were the dominant phytoplankton group throughout the mesocosm incubation period, but the proportion of dinoflagellates increased in low O2 mesocosms under both ambient and elevated CO2 levels when nutrients, especially silicate (used for cell wall biosynthesis in diatoms), were depleted. This was neat, with the observation also relating to Rubisco properties,  as the form II Rubisco found in dinoflagellates has a low specificity for CO2 over O2, which could make them more likely than other algal groups to benefit from decreased O2.

Results from the mesocosm experiment were inspiring as they coincided with results from the field investigation in the Pearl River estuary and our hypothesis linking decreased DO to improved primary productivity. To further investigate the mechanisms contributing to this we conducted a laboratory culture experiment to investigate photosynthetic performance, growth rate, and efficiency of CO2 concentrating mechanisms (CCMs) in the globally distributed coastal diatom Thalassiosira weissflogii incubated under four O2/CO2 combinations. As predicted, reduced levels of DO in the cultured T. weissflogii stimulated growth rate, enhanced photosynthetic performance, but reduced rates of mitochondrial respiration as well as photorespiration associated with Rubisco oxygenase activity.

With progressive ocean climate changes, deteriorating ocean deoxygenation is believed to disrupt the balance between O2 availability and metabolic O2 demand of some marine biota and impact heterotrophic processes. In our study, however, using data from natural phytoplankton assemblages, manipulated mesocosms and cultures of the diatom T. weissflogii,  we have been able to show that primary producers benefited from reduced O2 concentrations that were low enough to be detrimental for most marine animals. Even under elevated CO2 conditions, low O2-enhanced photosynthesis can potentially accelerate ‘re-oxygenation’ in illuminated waters, and thus may alleviate the impacts of diminished oxygen on animals. 

Simplified illustration of low O2-enhanced CCMs activity and subsequently increased re-oxygenation due to global deoxygenation and/or in intruded hypoxic waters.

Simplified illustration of low O2-enhanced CCMs activity and subsequently increased re-oxygenation due to global deoxygenation and/or in intruded hypoxic waters. Black, red, and blue arrows indicate directions, increase and decrease, respectively.

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Jia-Zhen Sun

PhD candidate, Xiamen University