Statistics of C3/C4-pathway related enzymes of
Abstract
Due to the low CO2 concentration in seawater, macroalgae including Saccharina japonica have developed mechanisms for using the abundant external pool of HCO3− as an exogenous inorganic carbon (Ci) source. Otherwise, the high photosynthetic efficiency of some macroalgae indicates that they might possess CO2 concentrating mechanisms (CCMs) to elevate CO2 concentration intracellularly around the active site of ribulose-1, 5-bisphosphate carboxylase/oxygenase (RuBisCo). As the photosynthetic modes of macroalgae are diverse (C3, C4 or a combination of C3 and C4 pathway), CCMs in different carbon fixation pathways should vary correspondingly. However, both in C3 and C4 pathways, carbonic anhydrase (CA) plays a key role by supplying either CO2 to RuBisCO or HCO3− to PEPC. Over the past decade, although CA activities have been detected in a number of macroalgae, genes of CA family, expression levels of CA genes under different CO2 concentrations, as well as subcellular location of each CA have been rarely reported. Based on analysis the reported high-throughput sequencing data of S. japonica, 12 CAs of S. japonica (SjCA) genes were obtained. Neighbor-Joining (NJ) phylogenetic tree of SjCAs constructed using Mega6.0 and the subcellular location prediction of each CA by WoLFPSORT are also conducted in this article.
Keywords
- Macroalgae
- Inorganic carbon uptake
- C3 and C4 metabolism
- Carbonic anhydrase
- Saccharina japonica
1. Introduction
Kelps demonstrate high photosynthetic rates. According to the reports, productivity of large brown algae (e.g.,
The enzyme ribulose-1, 5-bisphosphate carboxylase/oxygenase (RuBisCo) is crucial in CO2 assimilation. This bifunctional enzyme could catalyse the initial steps of photosynthetic carbon reduction and photorespiratory carbon oxidation cycles by combining CO2 and O2 with ribulose-1, 5-bisphosphate (RuBP) [2, 3]. RuBP carboxylation determines the net photosynthetic efficiency of photoautotrophs [4]. However, RuBisCo has a surprisingly low affinity for CO2 and the oxygenase activity is intrinsic to RuBisCo. For kelps, the enzymatic efficiency of RuBisCo is also limited by the low concentration and diffusion coefficient of CO2 in seawater [5]. At a natural pH of about 8, the major part of the dissolved inorganic carbon (DIC) is in the form of bicarbonate (
2. Photosynthetic modes of macroalgae
As with terrestrial angiosperms where a single family may possess species with divergent photosynthetic modes [13], the marine macroalgal divisions also exhibit diversity. The photosynthetic carbon fixation pathways of marine macrophytic algae generally follow that of C3 plants [14]. However, for certain genera, a number of studies have shown photosynthesis to possess C4-like photosynthetic characteristics, including the high phosphoenolpyruvate carboxykinase (PEPCK) activity with low phosphoenolpyruvate carboxylase (PEPC) activity, little photorespiration and the labelling of malate and aspartate as an early product of carbon fixation. Based on this, it has been suggested that these macroalgae are of the C4 type, or a combination of C3 and C4, type [15–17], although Kremer and Küppers [18] had contradicted the decision whether a species is a C4 plant or not based only on chromatographic and enzymatic analysis. In recent decades, our understanding of the possible metabolic pathways of macroalgae has been extended with using the available sequencing resources and molecular technologies and applying molecular approaches. Reiskind et al. [19] reported that a limited C4-like system in the green alga
In C3 and C4 metabolisms, CO2 is the substrate of RuBisCo and assimilated through the Calvin cycle. In this cycle, CO2, catalysed with RuBisCo, combines with RuBP to form two molecules of 3-PGA. PGA is reduced to triose. RuBisCo, a bifunctional enzyme, may catalyse the combination of RuBP and CO2 for photosynthetic carbon reduction or may combine with O2 for C2 photorespiration [3]. The ratio of CO2 to O2 around RuBisCo is a major factor for the enzyme to choose the photosynthetic carbon reduction or C2 photorespiration carbon oxidation [26]. The low CO2 concentration around RuBisCo may not only impose restrictions on photosynthesis but also cause permanent light injuries to photosynthetic organelle [27–29]. The speciation of DIC (Ci) is pH dependent. Above pH 4.5, the proportion occurring as CO2 (aq) decreases and
Based on a series of reports on the presence of CCM in blue-green algae and
3. Inorganic carbon absorption mechanisms of macroalgae
The methods of CO2 and/or
The extent to which marine macroalgae are able to acquire
Thus, the CAext mechanism plays an important role in the CCM macroalgae absorption and the utilization of the relatively abundant
4. Ci transition process in CCMs of macroalgae
Ci acquisition mechanisms are extensively studied and well-known in microalgae [44, 38]. For instance, regardless of the Ci form (CO2 or
For C4 photosynthesis, CA is required to convert CO2 to
In conclusion, CA (CAext+CAint) is essential for the reversible
5. Carbonic anhydrase
CAs are metalloenzymes that catalyse the reversible interconversion of CO2 and
Conclusively, CAs, including CAext and CAint (Figure 1), play an important role in the transportation or concentration process of the Ci. And as for C3 and C4 metablisms have different carboxylase, CAs might play different roles in CCMs of macroalgae with different photosynthetic mode. Thus, isolating of the
6. Studies of S. japonica CCM
Photosynthesis modes | Enzyme names | Unigenes |
---|---|---|
C3-pathway | 23 | |
Glyceraldehyde-3-phosphate dehydrogenase (phosphorylating) (GAPDH) | 4 | |
Transketolase | 1 | |
Phosphoribulokinase | 2 | |
Phosphoglycerate kinase (PGK) | 5 | |
Fructose-1,6-bisphosphatase (FBPase) | 1 | |
Sedoheptulose-bisphosphatase (SBPase) | 3 | |
Fructose-bisphosphate aldolase | 1 | |
Ribulose-phosphate 3-epimerase | 2 | |
Triose-phosphate isomerase (TIM) | 1 | |
Ribose-5-phosphate isomerase | 1 | |
Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo), small | 1 | |
Ribulose-1,5-bisphosphate carboxylase/oxygenase(RuBisCo), large | 1 | |
C4-pathway | 16 | |
Malate dehydrogenase | 4 | |
Aspartate aminotransferase (AST) | 4 | |
Pyruvate kinase | 4 | |
Phosphoenolpyruvate carboxylase (PEPC) | 1 | |
Phosphoenolpyruvate carboxykinase (PEPCK) | 1 | |
Pyruvate phosphate dikinase | 1 | |
Arginine/alanine aminopeptidase | 1 | |
Total | 39 |
Considering CAs play key roles in CCMs of macroalgae, it is important to determine the numbers and characterizations of CA genes of
Enzyme | Gene IDa | AA no. | Full length (Y/N) | Subcellular location prediction |
---|---|---|---|---|
Sj |
JF827608 | 290 | Y | Chloroplast and thylakoid membrane [93] |
Sj |
SJ07762 | 205 | N | Secreted |
Sj |
SJ07765 | 160 | N | Cytoplasmic |
Sj |
SJ13238 | 151 | N | Cytoplasmic |
Sj |
SJ13240 | 294 | N | Mitochondrial inner membrane |
Sj |
SJ18135 | 257 | N | Cytoplasmic |
Sj |
SJ18141 | 189 | N | Cytoplasmic |
Sj |
SJ12311 | 314 | Y | Chloroplast thylakoid membrane |
Sj |
SJ17783 | 307 | Y | Mitochondrial |
Sj |
SJ07587 | 305 | N | Cytoplasmic |
Sj |
SJ22175 | 161 | N | Mitochondrial |
Sj |
SJ21158 | 246 | N | Chloroplast |
The completion of the CCM modelling of sporophyte and gametophyte in
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