Plastid-localized xanthorhodopsin increases diatom biomass and ecosystem productivity in iron-limited surface oceans

Strauss, Jan, Deng, Longji, Gao, Shiqiang, Toseland, Andrew, Bachy, Charles, Zhang, Chong, Kirkham, Amy, Hopes, Amanda, Utting, Robert, Joest, Eike F., Tagliabue, Alessandro, Löw, Christian, Worden, Alexandra Z., Nagel, Georg and Mock, Thomas ORCID: https://orcid.org/0000-0001-9604-0362 (2023) Plastid-localized xanthorhodopsin increases diatom biomass and ecosystem productivity in iron-limited surface oceans. Nature Microbiology, 8 (11). pp. 2050-2066. ISSN 2058-5276

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Abstract

Microbial rhodopsins are photoreceptor proteins that convert light into biological signals or energy. Proteins of the xanthorhodopsin family are common in eukaryotic photosynthetic plankton including diatoms. However, their biological role in these organisms remains elusive. Here we report on a xanthorhodopsin variant (FcR1) isolated from the polar diatom Fragilariopsis cylindrus. Applying a combination of biophysical, biochemical and reverse genetics approaches, we demonstrate that FcR1 is a plastid-localized proton pump which binds the chromophore retinal and is activated by green light. Enhanced growth of a Thalassiora pseudonana gain-of-function mutant expressing FcR1 under iron limitation shows that the xanthorhodopsin proton pump supports growth when chlorophyll-based photosynthesis is iron-limited. The abundance of xanthorhodopsin transcripts in natural diatom communities of the surface oceans is anticorrelated with the availability of dissolved iron. Thus, we propose that these proton pumps convey a fitness advantage in regions where phytoplankton growth is limited by the availability of dissolved iron.

Item Type:	Article
Additional Information:	Funding information: The PhD studentship of J.S. was funded by the School of Environmental Sciences at UEA. Funding was further provided by grants from the Natural Environment Research Council (NE/I001751/1 to T.M. and NE/K013734/1 to T.M. and J.S.). J.S. was additionally supported by a fellowship from the EMBL Interdisciplinary Postdoc (EIPOD) programme under the Marie Sklodowska-Curie Actions COFUND programme (grant number 664726), GEOMAR Helmholtz Centre for Ocean Research Kiel and the Gordon and Betty Moore Foundation (Grant 3788) to A.Z.W. G.N. acknowledges support from the Louis-Jeantet Prize for medicine.
Faculty \ School:	Faculty of Science > School of Environmental Sciences Faculty of Science > School of Biological Sciences Faculty of Science University of East Anglia Research Groups/Centres > Theme - ClimateUEA
UEA Research Groups:	Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation Faculty of Science > Research Groups > Centre for Ocean and Atmospheric Sciences Faculty of Science > Research Groups > Environmental Biology
Related URLs:	https://www.nature.com/articles/s41564-0...
Depositing User:	LivePure Connector
Date Deposited:	11 Mar 2024 09:31
Last Modified:	10 Dec 2024 01:43
URI:	https://ueaeprints.uea.ac.uk/id/eprint/94612
DOI:	10.1038/s41564-023-01498-5

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