Adaptive thermostability of light-harvesting complexes in marine picocyanobacteria (2024)

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Justine Pittera

Sorbonne Universités, Université Pierre and Marie Curie (Paris 06), UMR 7144, Marine Phototrophic Prokaryotes (MaPP) Team

, Roscoff Cedex 29688,

France

Centre National de la Recherche Scientifique, UMR 7144, Marine Plankton Group, Station Biologique

, Roscoff Cedex,

France

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,

Frédéric Partensky

Sorbonne Universités, Université Pierre and Marie Curie (Paris 06), UMR 7144, Marine Phototrophic Prokaryotes (MaPP) Team

, Roscoff Cedex 29688,

France

Centre National de la Recherche Scientifique, UMR 7144, Marine Plankton Group, Station Biologique

, Roscoff Cedex,

France

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Christophe Six

Sorbonne Universités, Université Pierre and Marie Curie (Paris 06), UMR 7144, Marine Phototrophic Prokaryotes (MaPP) Team

, Roscoff Cedex 29688,

France

Centre National de la Recherche Scientifique, UMR 7144, Marine Plankton Group, Station Biologique

, Roscoff Cedex,

France

Correspondence: C Six, UMR 7144 UPMC-CNRS, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, France. E-mail: christophe.six@sb-roscoff.fr

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The ISME Journal, Volume 11, Issue 1, January 2017, Pages 112–124, https://doi.org/10.1038/ismej.2016.102

Published:

26 July 2016

Article history

Received:

21 December 2015

Revision received:

21 April 2016

Accepted:

24 April 2016

Published:

26 July 2016

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    Justine Pittera, Frédéric Partensky, Christophe Six, Adaptive thermostability of light-harvesting complexes in marine picocyanobacteria, The ISME Journal, Volume 11, Issue 1, January 2017, Pages 112–124, https://doi.org/10.1038/ismej.2016.102

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Abstract

Marine Synechococcus play a key role in global oceanic primary productivity. Their wide latitudinal distribution has been attributed to the occurrence of lineages adapted to distinct thermal niches, but the physiological and molecular bases of this ecotypic differentiation remain largely unknown. By comparing six strains isolated from different latitudes, we showed that the thermostability of their light-harvesting complexes, called phycobilisomes (PBS), varied according to the average sea surface temperature at strain isolation site. Comparative analyses of thermal unfolding curves of the three phycobiliproteins (PBP) constituting PBS rods suggested that the differences in thermostability observed on whole PBSs relied on the distinct molecular flexibility and stability of their individual components. Phycocyanin was the least thermostable of all rod PBP, constituting a fragility point of the PBS under heat stress. Amino-acid composition analyses and structural hom*ology modeling notably revealed the occurrence of two amino-acid substitutions, which might have a role in the observed differential thermotolerance of this phycobiliprotein among temperature ecotypes. We hypothesize that marine Synechococcus ancestors occurred first in warm niches and that during the colonization of cold, high latitude thermal niches, their descendants have increased the molecular flexibility of PBP to maintain optimal light absorption capacities, this phenomenon likely resulting in a decreased stability of these proteins. This apparent thermoadaptability of marine Synechococcus has most probably contributed to the remarkable ubiquity of these picocyanobacteria in the ocean.

© International Society for Microbial Ecology 2017

This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/pages/standard-publication-reuse-rights)

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