A SLC4 family bicarbonate transporter is critical for intracellular pH regulation and biomineralization in sea urchin embryos

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Abstract

Efficient pH regulation is a fundamental requisite of all calcifying systems in animals and plants but with the underlying pH regulatory mechanisms remaining largely unknown. Using the sea urchin larva this work identified the SLC4 HCO₃^- transporter family member SpSlc4a10 to be critically involved in the formation of an elaborate calcitic endoskeleton. SpSlc4a10 is specifically expressed by calcifying primary mesenchyme cells with peak expression during de novo formation of the skeleton. Knock-down of SpSlc4a10 led to pH regulatory defects accompanied by decreased calcification rates and skeleton deformations. Reductions in seawater pH, resembling ocean acidification scenarios, led to an increase in SpSlc4a10 expression suggesting a compensatory mechanism in place to maintain calcification rates. We propose a first pH regulatory and HCO₃^- concentrating mechanism that is fundamentally linked to the biological precipitation of CaCO₃. This knowledge will help understanding biomineralization strategies in animals and their interaction with a changing environment.

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All data generated or analysed during this study are included in the manuscript and supporting files.

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Marian Y Hu

Institute of Physiology, Christian-Albrechts University of Kiel, Kiel, Germany

For correspondence
m.hu@physiologie.uni-kiel.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8914-139X
Jia-jiun Yan

Institute of Physiology, Christian-Albrechts University of Kiel, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.
Inga Petersen

Institute of Physiology, Christian-Albrechts University of Kiel, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.
Nina Himmerkus

Institute of Physiology, Christian-Albrechts University of Kiel, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.
Markus Bleich

Institute of Physiology, Christian-Albrechts University of Kiel, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.
Meike Stumpp

Comparative Immunobiology, Institute of Zoology, Christian-Albrechts University of Kiel, Kiel, Germany

Competing interests
The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (Cluster of Excellence CP1519)

Marian Y Hu

Deutsche Forschungsgemeinschaft (Cluster of Excellence CP1409)

Marian Y Hu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.