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Enzyme adaptation to habitat thermal legacy shapes the thermal plasticity of marine microbiomes

Marasco, Ramona; Fusi, Marco; Coscolín, Cristina; Barozzi, Alan; Almendral, David; Bargiela, Rafael; Nutschel, Christina Gohlke neé; Pfleger, Christopher; Dittrich, Jonas; Gohlke, Holger; Matesanz, Ruth; Sanchez-Carrillo, Sergio; Mapelli, Francesca; Chernikova, Tatyana N.; Golyshin, Peter N.; Ferrer, Manuel; Daffonchio, Daniele

Authors

Ramona Marasco

Marco Fusi

Cristina Coscolín

Alan Barozzi

David Almendral

Rafael Bargiela

Christina Gohlke neé Nutschel

Christopher Pfleger

Jonas Dittrich

Holger Gohlke

Ruth Matesanz

Sergio Sanchez-Carrillo

Francesca Mapelli

Tatyana N. Chernikova

Peter N. Golyshin

Manuel Ferrer

Daniele Daffonchio



Abstract

Microbial communities respond to temperature with physiological adaptation and compositional turnover. Whether thermal selection of enzymes explains marine microbiome plasticity in response to temperature remains unresolved. By quantifying the thermal behaviour of seven functionally-independent enzyme classes (esterase, extradiol dioxygenase, phosphatase, beta-galactosidase, nuclease, transaminase, and aldo-keto reductase) in native proteomes of marine sediment microbiomes from the Irish Sea to the southern Red Sea, we record a significant effect of the mean annual temperature (MAT) on enzyme response in all cases. Activity and stability profiles of 228 esterases and 5 extradiol dioxygenases from sediment and seawater across 70 locations worldwide validate this thermal pattern. Modelling the esterase phase transition temperature as a measure of structural flexibility confirms the observed relationship with MAT. Furthermore, when considering temperature variability in sites with non-significantly different MATs, the broadest range of enzyme thermal behaviour and the highest growth plasticity of the enriched heterotrophic bacteria occur in samples with the widest annual thermal variability. These results indicate that temperature-driven enzyme selection shapes microbiome thermal plasticity and that thermal variability finely tunes such processes and should be considered alongside MAT in forecasting microbial community thermal response.

Journal Article Type Article
Acceptance Date Feb 8, 2023
Online Publication Date Feb 24, 2023
Publication Date 2023
Deposit Date Feb 27, 2023
Publicly Available Date Feb 27, 2023
Journal Nature Communications
Publisher Nature Publishing Group
Peer Reviewed Peer Reviewed
Volume 14
Issue 1
Article Number 1045
DOI https://doi.org/10.1038/s41467-023-36610-0

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Copyright Statement
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.




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