Abstract
BackgroundPyropia yezoensis (Rhodophyta) is widely cultivated in East Asia and plays important economic, ecological and research roles. Although inorganic carbon utilization of P. yezoensis has been investigated from a physiological aspect, the carbon concentration mechanism (CCM) of P. yezoensis remains unclear. To explore the CCM of P. yezoensis, especially during its different life stages, we tracked changes in the transcriptome, photosynthetic efficiency and in key enzyme activities under different inorganic carbon concentrations.ResultsPhotosynthetic efficiency demonstrated that sporophytes were more sensitive to low carbon (LC) than gametophytes, with increased photosynthesis rate during both life stages under high carbon (HC) compared to normal carbon (NC) conditions. The amount of starch and number of plastoglobuli in cells corresponded with the growth reaction to different inorganic carbon (Ci) concentrations. We constructed 18 cDNA libraries from 18 samples (three biological replicates per Ci treatment at two life cycles stages) and sequenced these using the Illumina platform. De novo assembly generated 182,564 unigenes, including approximately 275 unigenes related to CCM. Most genes encoding internal carbonic anhydrase (CA) and bicarbonate transporters involved in the biophysical CCM pathway were induced under LC in comparison with NC, with transcript abundance of some PyCAs in gametophytes typically higher than that in sporophytes. We identified all key genes participating in the C4 pathway and showed that their RNA abundances changed with varying Ci conditions. High decarboxylating activity of PEPCKase and low PEPCase activity were observed in P. yezoensis. Activities of other key enzymes involved in the C4-like pathway were higher under HC than under the other two conditions. Pyruvate carboxylase (PYC) showed higher carboxylation activity than PEPC under these Ci conditions. Isocitrate lyase (ICL) showed high activity, but the activity of malate synthase (MS) was very low.ConclusionWe elucidated the CCM of P. yezoensis from transcriptome and enzyme activity levels. All results indicated at least two types of CCM in P. yezoensis, one involving CA and an anion exchanger (transporter), and a second, C4-like pathway belonging to the PEPCK subtype. PYC may play the main carboxylation role in this C4-like pathway, which functions in both the sporophyte and gametophyte life cycles.
Highlights
Pyropia yezoensis (Rhodophyta) is widely cultivated in East Asia and plays important economic, ecological and research roles
Under low carbon (LC), photosynthetic efficiency was around 17.75 ± 0.1% lower than that under normal carbon (NC), while it was enhanced by about 14.11 ± 0.08% under high carbon (HC) compared with NC, as indicated by changes in photosystem II (YII) (Fig. 2)
Photosynthetic efficiency was almost 5.91 ± 0.07% lower under LC than under NC, while it was enhanced by 16.77 ± 0.08% under HC compared with that under NC (Fig. 2)
Summary
Pyropia yezoensis (Rhodophyta) is widely cultivated in East Asia and plays important economic, ecological and research roles. Inorganic carbon utilization of P. yezoensis has been investigated from a physiological aspect, the carbon concentration mechanism (CCM) of P. yezoensis remains unclear. Due to the low amount of CO2 in seawater, most macroalgae have evolved a carbon concentrating mechanism (CCM) to utilize HCO3− for maintaining high levels of growth [5,6,7]; these CCMs are increasingly important because rising CO2 in the air has led to rising levels of HCO3− in water over the past few decades [8, 9]. Economic and cultural importance of macroalgae, we know relatively little about their CCMs. Various types of CCMs have been discovered in terrestrial plants and microalgae: biophysical, biochemical and basal CCM, respectively. Mitochondrial γ-CAs and NADH–ubiquinone oxidoreductase complex I are the main components in basal CCM [11, 12]
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