Role of C4 carbon fixation in Ulva prolifera, the macroalga responsible for the world\u2019s largest green tides

Dongyan Liu,Qian Ma,Donald M Anderson,Ivan Valiela,Xiyan Sun,John K Keesing,Kunshan Gao,Yu Zhen,Yujue Wang

doi:10.1038/s42003-020-01225-4

Abstract

Most marine algae preferentially assimilate CO2 via the Calvin-Benson Cycle (C3) and catalyze HCO3− dehydration via carbonic anhydrase (CA) as a CO2-compensatory mechanism, but certain species utilize the Hatch-Slack Cycle (C4) to enhance photosynthesis. The occurrence and importance of the C4 pathway remains uncertain, however. Here, we demonstrate that carbon fixation in Ulva prolifera, a species responsible for massive green tides, involves a combination of C3 and C4 pathways, and a CA-supported HCO3− mechanism. Analysis of CA and key C3 and C4 enzymes, and subsequent analysis of δ13C photosynthetic products showed that the species assimilates CO2 predominately via the C3 pathway, uses HCO3− via the CA mechanism at low CO2 levels, and takes advantage of high irradiance using the C4 pathway. This active and multi-faceted carbon acquisition strategy is advantageous for the formation of massive blooms, as thick floating mats are subject to intense surface irradiance and CO2 limitation.

Highlights

Most marine algae preferentially assimilate CO2 via the Calvin-Benson Cycle (C3) and catalyze HCO3− dehydration via carbonic anhydrase (CA) as a CO2-compensatory mechanism, but certain species utilize the Hatch-Slack Cycle (C4) to enhance photosynthesis
Consistent with this, the involvement of the C4 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 C4-related enzyme pyruvate orthophosphate dikinase (PPDKase)[15]; and (2) tissue δ13C range of U. prolifera (−21.9 to −14.9‰) at 16 stations in the Yellow Sea indicated a mix of C3 and C4 pathways in carbon fixation[16]
The patterns of C3 and C4 enzymes differed in response to variations in diurnal sunlight (Fig. 2): mean Rubisco activity was maximal in the morning (10:00 h) but declined significantly from 274 to 57 nmol · min−1 · g · fresh weight−1 at noon (12:00) under high light intensity (Tukey HSD = 5.327, crit. = 3.541, p = 0.001), and stayed low activity between 12:00 and 14:00 h, but increased significantly again from 42 to 143 nmol · min−1 · g · fresh weight−1 (Tukey HSD = 4.002, crit. = 3.541, p = 0.019) between 14:00 and 16:00 under reduced light intensity (Fig. 2a)

Summary

Introduction

Most marine algae preferentially assimilate CO2 via the Calvin-Benson Cycle (C3) and catalyze HCO3− dehydration via carbonic anhydrase (CA) as a CO2-compensatory mechanism, but certain species utilize the Hatch-Slack Cycle (C4) to enhance photosynthesis. Growth rates in the field were generally higher than 28% per day at temperatures greater than 20 °C14, and aerial cover of floating canopies exceed 30,000 km[2] across the Yellow Sea. Consistent with this, the involvement of the C4 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 C4-related enzyme pyruvate orthophosphate dikinase (PPDKase)[15]; and (2) tissue δ13C range of U. prolifera (−21.9 to −14.9‰) at 16 stations in the Yellow Sea indicated a mix of C3 and C4 pathways in carbon fixation[16]

Methods

Results

Conclusion