Ciliary flows in corals ventilate target areas of high photosynthetic oxygen production

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Most tropical corals live in symbiosis with Symbiodiniaceae algae whose photosynthetic production of oxygen (O2) may lead to excess O2 in the diffusive boundary layer (DBL) above the coral surface. When flow is low, cilia-induced mixing of the coral DBL is vital to remove excess O2 and prevent oxidative stress that may lead to coral bleaching and mortality. Here, we combined particle image velocimetry using O2-sensitive nanoparticles (sensPIV) with chlorophyll (Chla)-sensitive hyperspectral imaging to visualize the microscale distribution and dynamics of ciliary flows and O2 in the coral DBL in relation to the distribution of Symbiodiniaceae Chla in the tissue of the reef building coral, Porites lutea. Curiously, we found an inverse relation between O2 in the DBL and Chla in the underlying tissue, with patches of high O2 in the DBL above low Chla in the underlying tissue surrounding the polyp mouth areas and pockets of low O2 concentrations in the DBL above high Chla in the coenosarc tissue connecting neighboring polyps. The spatial segregation of Chla and O2 is related to ciliary-induced flows, causing a lateral redistribution of O2 in the DBL. In a 2D transport-reaction model of the coral DBL, we show that the enhanced O2 transport allocates parts of the O2 surplus to areas containing less chla, which minimizes oxidative stress. Cilary flows thus confer a spatially complex mass transfer in the coral DBL, which may play an important role in mitigating oxidative stress and bleaching in corals.
OriginalsprogEngelsk
TidsskriftCurrent Biology
Vol/bind32
Udgave nummer19
Sider (fra-til)4150-4158.e3
Antal sider13
ISSN0960-9822
DOI
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
We thank Esther Lüdtke and Ulrike Holtz for their help with the culturing of the coral colonies, Dr. Arjun Chennu (ZMT) for providing the hyperspectral camera, and Paul Faerber for technical support. This research was conducted in the framework of the PhD project of C.O.P. at the University of Bremen and the Alfred Wegener Institute (AWI). It was supported and financed by FONDECYT , an initiative from the Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica (CONCYTEC), Perú , Contrato 086-2016-FONDECYT and the AWI (PoF4.6: Marine and Polar Life). MPI-MM Bremen provided logistic and instrumental support. S.A. acknowledges funding from the Max Planck Society (MPG). K.K. acknowledges funding from the Grundfos Foundation and a Sapere Aude grant from the Independent Research Fund Denmark (IRFD): DFF-8048-00057B .

Funding Information:
We thank Esther Lüdtke and Ulrike Holtz for their help with the culturing of the coral colonies, Dr. Arjun Chennu (ZMT) for providing the hyperspectral camera, and Paul Faerber for technical support. This research was conducted in the framework of the PhD project of C.O.P. at the University of Bremen and the Alfred Wegener Institute (AWI). It was supported and financed by FONDECYT, an initiative from the Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica (CONCYTEC), Perú, Contrato 086-2016-FONDECYT and the AWI (PoF4.6: Marine and Polar Life). MPI-MM Bremen provided logistic and instrumental support. S.A. acknowledges funding from the Max Planck Society (MPG). K.K. acknowledges funding from the Grundfos Foundation and a Sapere Aude grant from the Independent Research Fund Denmark (IRFD): DFF-8048-00057B. C.O.P. S.A. C.R. and M.H. designed the experiments for this study. C.O.P. conducted all the experiments. C.O.P. and S.A. analyzed the sensPIV and hyperspectral data and generated the result figures. M.H. and S.A. worked on the model and its figures. K.K. created and supplied the sensPIV particles necessary for the oxygen experiments. C.O.P. S.A. K.K. C.R. and M.H. contributed to the interpretation of the collected data and conceived and wrote the manuscript. The authors declare no competing interests.

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