Evolutionarily distinct strategies for the acquisition of inorganic carbon from seawater in marine diatoms

Tsuji, Yoshinori; Mahardika, Anggara; Matsuda, Yusuke

doi:10.1093/jxb/erx102

Cited by 35 publications

(25 citation statements)

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“…, Tsuji et al. ). The catalytic rate of CAs has been suggested to be generally pH‐dependent, and the maximal k cat of the enzymes are achieved under alkaline conditions (Xu et al.…”

Section: Discussionmentioning

confidence: 99%

“…They are enzymes that catalyze the conversion of HCO 3 À to CO 2 at the cell surface and thus play a critical role in supplying Ci for photosynthesis (Moroney et al 2011, Hopkinson et al 2013). Among the three species studied here, there is currently no molecular evidence for eCAs in Phaeodactylum tricornutum , Samukawa et al 2014; Thalassiosira pseudonana contains eCAs (i.e., dCA1 and fCA1) located at the periplasmic space outside the cells and serve to convert HCO 3 À to CO 2 to facilitate the usage of HCO 3 À , Samukawa et al 2014; although Chaetoceros muelleri expresses eCA, these do not seem to play a primary role in Ci acquisition (Shen and Hopkinson 2015, Smith-Harding et al 2017, Tsuji et al 2017. The catalytic rate of CAs has been suggested to be generally pH-dependent, and the maximal k cat of the enzymes are achieved under alkaline conditions (Xu et al 2008, de Araujo et al 2014.…”

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confidence: 89%

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The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO₂ and pH

Shi

Hong

Shen

et al. 2019

Journal of Phycology

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Although increasing the pCO2 for diatoms will presumably down‐regulate the CO2‐concentrating mechanism (CCM) to save energy for growth, different species have been reported to respond differently to ocean acidification (OA). To better understand their growth responses to OA, we acclimated the diatoms Thalassiosira pseudonana, Phaeodactylum tricornutum, and Chaetoceros muelleri to ambient (pCO2 400 μatm, pH 8.1), carbonated (pCO2 800 μatm, pH 8.1), acidified (pCO2 400 μatm, pH 7.8), and OA (pCO2 800 μatm, pH 7.8) conditions and investigated how seawater pCO2 and pH affect their CCMs, photosynthesis, and respiration both individually and jointly. In all three diatoms, carbonation down‐regulated the CCMs, while acidification increased both the photosynthetic carbon fixation rate and the fraction of CO2 as the inorganic carbon source. The positive OA effect on photosynthetic carbon fixation was more pronounced in C. muelleri, which had a relatively lower photosynthetic affinity for CO2, than in either T. pseudonana or P. tricornutum. In response to OA, T. pseudonana increased respiration for active disposal of H+ to maintain its intracellular pH, whereas P. tricornutum and C. muelleri retained their respiration rate but lowered the intracellular pH to maintain the cross‐membrane electrochemical gradient for H+ efflux. As the net result of changes in photosynthesis and respiration, growth enhancement to OA of the three diatoms followed the order of C. muelleri > P. tricornutum > T. pseudonana. This study demonstrates that elucidating the separate and joint impacts of increased pCO2 and decreased pH aids the mechanistic understanding of OA effects on diatoms in the future, acidified oceans.

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“…, Tsuji et al. ). The catalytic rate of CAs has been suggested to be generally pH‐dependent, and the maximal k cat of the enzymes are achieved under alkaline conditions (Xu et al.…”

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 89%

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO₂ and pH

Shi

Hong

Shen

et al. 2019

Journal of Phycology

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“…Some diatoms also possess extracellular carbonic anhydrase (CA), which allows the rapid formation of CO 2 from abundant HCO 3 − in the periplasmic space and may provide cells a nearly unlimited supply of CO 2 (Martin and Tortell, 2008;Hopkinson et al, 2011;Samukawa et al, 2014). Tsuji et al (2017) demonstrated that some evolutionarily distant marine diatoms mainly take up CO 2 formed from HCO 3 − by external CA. However, the mechanisms that support the efficient movement of CO 2 across the plasma membrane and four-layered membranes of secondary plastids have yet to be clarified.…”

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confidence: 99%

Plasma-membrane-type aquaporins from marine diatoms function as CO2/NH3 channels and provide photoprotection

et al. 2018

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Aquaporins (AQPs) are ubiquitous water channels that facilitate the transport of many small molecules and may play multiple vital roles in aquatic environments. In particular, mechanisms to maintain transmembrane fluxes of important small molecules have yet to be studied in marine photoautotrophic organisms. Here, we report the occurrence of multiple AQPs with differential cellular localizations in marine diatoms, an important group of oceanic primary producers. The AQPs play a role in mediating the permeability of membranes to CO and NH In silico surveys revealed the presence of five AQP orthologs in the pennate diatom and two in the centric diatom GFP fusions of putative AQPs displayed clear localization to the plasma membrane (PtAGP1 and PtAQP2), the chloroplast endoplasmic reticulum (CER; PtAGP1 and PtAQP3), and the tonoplast (PtAQP5) in In, GFP-AQP fusion proteins were found on the vacuole membrane (TpAQP1) and CER (TpAQP2). Transcript levels of both and were highly induced by ammonia, while only was induced by high (1%[v/v]) CO Constitutive overexpression of GFP-tagged PtAQP1 and PtAQP2 significantly increased CO and NH permeability in , strongly indicating that these AQPs function in regulating CO/NH permeability in the plasma membrane and/or CER. Cells carrying GFP-tagged PtAQP1 and PtAQP2 had higher nonphotochemical quenching under high light relative to that of wild-type cells, suggesting that these AQPs are involved in photoprotection. These AQPs may facilitate the efflux of NH, preventing the uncoupling effect of high intracellular ammonia concentrations.

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“…Similarly, a recent study by Tsuji et al. () found no impact of AZ on the K 0.5 C i or V max for photosynthetic O 2 evolution in air‐bubbled cultures of C. muelleri . Together, these findings suggest that CA ext ‐mediated uptake of C i is only induced at very low CO 2 concentrations in this species.…”

Section: Discussionmentioning

confidence: 62%

The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri

Smith-Harding

Beardall

Mitchell

2017

Journal of Phycology

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Carbon dioxide concentrating mechanisms (CCMs) act to improve the supply of CO at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase. There is substantial evidence that in some microalgal species CCMs involve an external carbonic anhydrase (CA ) and that CA activity is induced by low CO concentrations in the growth medium. However, much of this work has been conducted on cells adapted to air-equilibrium concentrations of CO , rather than to changing CO conditions caused by growing microalgal populations. We investigated the role of CA in inorganic carbon (C ) acquisition and photosynthesis at three sampling points during the growth cycle of the cosmopolitan marine diatom Chaetoceros muelleri. We observed that CA activity increased with decreasing C , particularly CO , concentration, supporting the idea that CA is modulated by external CO concentration. Additionally, we found that the contribution of CA activity to carbon acquisition for photosynthesis varies over time, increasing between the first and second sampling points before decreasing at the last sampling point, where external pH was high. Lastly, decreases in maximum quantum yield of photosystem II (F /F ), chlorophyll, maximum relative electron transport rate, light harvesting efficiency (α) and maximum rates of C - saturated photosynthesis (V ) were observed over time. Despite this decrease in photosynthetic capacity an up-regulation of CCM activity, indicated by a decreasing half-saturation constant for CO (K CO ), occurred over time. The flexibility of the CCM during the course of growth in C. muelleri may contribute to the reported dominance and persistence of this species in phytoplankton blooms.

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Evolutionarily distinct strategies for the acquisition of inorganic carbon from seawater in marine diatoms

Abstract: The uptake of dissolved inorganic carbon by marine diatoms is facilitated by solute carrier transporters or external carbonic anhydrases. The occurrence of these distinct strategies is unrelated to phylogeny.

Cited by 35 publications

References 59 publications

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO₂ and pH

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO₂ and pH

Plasma-membrane-type aquaporins from marine diatoms function as CO2/NH3 channels and provide photoprotection

The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri

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Evolutionarily distinct strategies for the acquisition of inorganic carbon from seawater in marine diatoms

Abstract: The uptake of dissolved inorganic carbon by marine diatoms is facilitated by solute carrier transporters or external carbonic anhydrases. The occurrence of these distinct strategies is unrelated to phylogeny.

Cited by 35 publications

References 59 publications

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO2 and pH

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO2 and pH

Plasma-membrane-type aquaporins from marine diatoms function as CO2/NH3 channels and provide photoprotection

The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri

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The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO₂ and pH

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO₂ and pH