Stable isotopic evidence of nitrogen sources and C4 metabolism driving the world’s largest macroalgal green tides in the Yellow Sea

Abstract

During recent years, rapid seasonal growth of macroalgae covered extensive areas within the Yellow Sea, developing the world’s most spatially extensive “green tide”. The remarkably fast accumulation of macroalgal biomass is the joint result of high nitrogen supplies in Yellow Sea waters, plus ability of the macroalgae to optionally use C4 photosynthetic pathways that facilitate rapid growth. Stable isotopic evidence shows that the high nitrogen supply is derived from anthropogenic sources, conveyed from watersheds via river discharges, and by direct atmospheric deposition. Wastewater and manures supply about half the nitrogen used by the macroalgae, fertiliser and atmospheric deposition each furnish about a quarter of the nitrogen in macroalgae. The massive green tides affecting the Yellow Sea are likely to increase, with significant current and future environmental and human consequences. Addressing these changing trajectories will demand concerted investment in new basic and applied research as the basis for developing management policies.

Regional variation in δ13C of coral reef macroalgae

“…), the enzyme that fixes CO 2 in photosynthesis, thereby enhancing productivity. In almost all cases the biochemistry of photosynthesis in macroalgae is C 3 : while there is one verified C 4 marine macroalga ( Udotea flabellum ) (Koch et al ), claims that others, for example, Ulva , are facultative C 4 based on δ 13 C (Valiela et al ), are not supported by other data (Beer and Israel ). Most evidence is consistent with biophysical CCMs in marine macroalgae, which depend on active transport of protons and/or bicarbonate (Giordano et al ; Raven and Hurd ; Raven and Giordano ).…”

Role of C4 carbon fixation in Ulva prolifera, the macroalga responsible for the world’s largest green tides

“…Large floating mats formed by U. prolifera block air-sea exchange, thus, HCO 3 − uptake and assimilation could become important for rapid biomass accumulation. This was reflected in the tissue δ 13 C (culture samples: −19.5 to −17.4‰; field samples: −21.9 to −14.9‰) 16 .…”

“…Coastal eutrophication and high light supply in the Yellow Sea are important environmental conditions that favor the initiation of C 4 function of U. prolifera . During the summer (June–August) when the U. prolifera bloom is forming, dissolved inorganic nitrogen (DIN) concentrations are 10–80 µM near the coast and 1–15 µM offshore 16 , and the average light intensity in surface seawaters is ~1072.2 µmol photons m −2 s −1 34 . In this study, the DIN concentrations in the culture medium were about 30 µM and the daily average light intensity on sunny days in experiments 1 and 3 was 1196 and 1011 µmol photons m −2 s −1 , respectively.…”

“…Growth rates in the field were generally higher than 28% per day at temperatures greater than 20°C 14 , and aerial cover of floating canopies exceed 30,000 km 2 across the Yellow Sea. Consistent with this, the involvement of the C 4 pathway in photosynthesis of U. prolifera has been suggested as an important mechanism to achieve such rapid biomass accumulation, based on two lines of evidence: (1) gene and enzyme analysis in U. prolifera revealed the existence and activity of the C 4 -related enzyme pyruvate orthophosphate dikinase (PPDKase) 15 ; and (2) tissue δ 13 C range of U. prolifera (−21.9 to −14.9‰) at 16 stations in the Yellow Sea indicated a mix of C 3 and C 4 pathways in carbon fixation 16 .…”

Photosynthetic responses ofHalimeda scabra(Chlorophyta, Bryopsidales) to interactive effects of temperature, pH, and nutrients and its carbon pathways

“…Values of δ 13 C between -30 and -10 indicate active uptake of both HCO 3 − and CO 2 and species whose fixation fall within this range are classified as species with active CCM (Maberly, Raven & Johnston, 1992;Raven et al, 2002;Diaz-Pulido et al, 2016;Bender-Champ, Diaz-Pulido & Dove, 2017). Species with δ 13 C signatures between −32 and −22 are considered as C3 plants while δ 13 C between −16 and -10 are typical for C4 plants (Valiela et al, 2018). Considering these ranges and the results obtained in this work, H. scabra could be classified as a C3 plant with a CCM that uses both, HCO 3 − and CO 2 as a resource of C i for photosynthesis.…”