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

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.

Citation

Marasco, R., Fusi, M., Coscolín, C., Barozzi, A., Almendral, D., Bargiela, R., Nutschel, C. G. N., Pfleger, C., Dittrich, J., Gohlke, H., Matesanz, R., Sanchez-Carrillo, S., Mapelli, F., Chernikova, T. N., Golyshin, P. N., Ferrer, M., & Daffonchio, D. (2023). Enzyme adaptation to habitat thermal legacy shapes the thermal plasticity of marine microbiomes. Nature Communications, 14(1), Article 1045. https://doi.org/10.1038/s41467-023-36610-0

• 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