SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater

Proc Natl Acad Sci U S A. 2013 Jan 29;110(5):1767-72. doi: 10.1073/pnas.1216234110. Epub 2013 Jan 7.

Abstract

Photosynthesis in marine diatoms is a vital fraction of global primary production empowered by CO(2)-concentrating mechanisms. Acquisition of HCO(3)(-) from seawater is a critical primary step of the CO(2)-concentrating mechanism, allowing marine photoautotrophic eukaryotes to overcome CO(2) limitation in alkaline high-salinity water. However, little is known about molecular mechanisms governing this process. Here, we show the importance of a plasma membrane-type HCO(3)(-) transporter for CO(2) acquisition in a marine diatom. Ten putative solute carrier (SLC) family HCO(3)(-) transporter genes were found in the genome of the marine pennate diatom Phaeodactylum tricornutum. Homologs also exist in marine centric species, Thalassiosira pseudonana, suggesting a general occurrence of SLC transporters in marine diatoms. Seven genes were found to encode putative mammalian-type SLC4 family transporters in P. tricornutum, and three of seven genes were specifically transcribed under low CO(2) conditions. One of these gene products, PtSLC4-2, was localized at the plasmalemma and significantly stimulated both dissolved inorganic carbon (DIC) uptake and photosynthesis in P. tricornutum. DIC uptake by PtSLC4-2 was efficiently inhibited by an anion-exchanger inhibitor, 4,4'-diisothiocyanostilbene-2,2'-disulfonic acid, in a concentration-dependent manner and highly dependent on Na(+) ions at concentrations over 100 mM. These results show that DIC influx into marine diatoms is directly driven at the plasmalemma by a specific HCO(3)(-) transporter with a significant halophilic nature.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid / pharmacology
  • Amino Acid Sequence
  • Bicarbonates / metabolism*
  • Biological Transport / drug effects
  • Carbon / metabolism
  • Carbon Dioxide / metabolism
  • Cell Membrane / metabolism
  • Diatoms / genetics
  • Diatoms / metabolism*
  • Diatoms / physiology
  • Dose-Response Relationship, Drug
  • Gene Expression
  • Kinetics
  • Membrane Transport Proteins / classification
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism*
  • Microscopy, Confocal
  • Models, Biological
  • Molecular Sequence Data
  • Photosynthesis / drug effects
  • Phylogeny
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Seawater / chemistry*
  • Sequence Homology, Amino Acid

Substances

  • Bicarbonates
  • Membrane Transport Proteins
  • Protein Isoforms
  • Carbon Dioxide
  • Carbon
  • 4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid

Associated data

  • GENBANK/AB733620
  • GENBANK/AB733621
  • GENBANK/AB733622
  • GENBANK/AB733623
  • GENBANK/AB733624