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Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana

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Abstract

Thirteen putative carbonic anhydrase (CA) genes have been identified in the marine multipolar centric diatom, Thalassiosira pseudonana, and two of these CAs have been localized previously. The first, an alpha CA (TpαCA1), was localized in the chloroplast stroma; the second, a zeta-type CA (TpζCA1), was localized to the periplasmic space. In the present study, cloning and localization of the remaining CAs were carried out. TpγCA2, TpγCA3, TpγCA4, TpγCA5, TpδCA1, TpδCA2, TpδCA3, and TpζCA1 were responsive to CO2 availability at the transcriptional level, being significantly reduced in cells grown at 0.4 % CO2, whereas TpαCA1, TpαCA2, TpαCA3, TpγCA1, and TpδCA4 transcript levels were constitutive with respect to CO2 concentration. Full-length cDNAs for TpγCA1, TpγCA2, TpγCA3, TpγCA4, TpδCA1, and TpδCA2 were isolated and fused with the enhanced-green fluorescent gene at their 3′ termini. These GFP-fusion constructs were transformed into T. pseudonana, and the resulting GFP fusion products were localized using fluorescence microscopy. The δ-type TpδCA1 was localized on the periphery of the cell, strongly suggesting localization to the periplasmic space or the frustule. The δ-type TpδCA3 and the γ-type TpγCA2 were, respectively, localized in a periplastidal compartment and the cytosol. The δ-type TpδCA2, and the γ-types TpγCA1, 3, and 4 were localized in the mitochondria. The distribution of CAs in T. pseudonana contrasts notably with that of the raphid pennate diatom P. tricornutum, with likely consequences for CCM function including modes of CO2 acquisition, regions in which DIC is accumulated, and needs for minimizing CO2 leakage from the chloroplast.

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Abbreviations

RubisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

CA:

Carbonic anhydrase

CER:

Chloroplast endoplasmic reticulum

PPC:

Periplastidal compartment

BLS:

Blob-like structure

CE:

Chloroplast envelope

CCM:

CO2 concentrating mechanism

DIC:

Dissolved-inorganic carbon

EZA:

Ethoxyzolamide

AZA:

Acetazolamide

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Acknowledgments

We thank Ms. Nobuko Higashiuchi for her technical assistance and Ms. Miyabi Inoue for her skillful secretarial assistance. This work was supported by the Grant-in-Aid for Scientific Research B (Grant No. 24310015 to Y. M.), by the Grant-in-Aid for Challenging Exploratory Research (Grant No. 24651119 to Y. M.) from Japan Society for the Promotion of Science (JSPS), by MEXT-Supported Program for the Strategic Research Foundation for the Advancement of Environmental Protection Technology and for Development of Intelligent Self-Organized Biomaterials, and by the US National Science Foundation (EF 1041034 and MCB 1129326 to B.H.).

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  1. Department of Bioscience, School of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda, Hyogo, 669-1337, Japan

    Mio Samukawa & Yusuke Matsuda

  2. Department of Marine Sciences, University of Georgia, Athens, GA, 30602-3636, USA

    Chen Shen & Brian M. Hopkinson

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  1. Mio Samukawa
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Correspondence to Yusuke Matsuda.

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M. Samukawa and S. Chen have contributed equally to this study.

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Samukawa, M., Shen, C., Hopkinson, B.M. et al. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana . Photosynth Res 121, 235–249 (2014). https://doi.org/10.1007/s11120-014-9967-x

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