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

Lookup NU author(s): Dr Marco FusiORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


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.


Publication metadata

Author(s): Marasco R, Fusi M, Coscolín C, Barozzi A, Almendral D, Bargiela R, Gohlke C, Pfleger C, Dittrich J, Gohlke H, Matesanz R, Sanchez-Carrillo S, Mapelli F, Chernikova TN, Golyshin PN, Ferrer M, Daffonchio D

Publication type: Article

Publication status: Published

Journal: Nature Communications

Year: 2023

Volume: 14

Online publication date: 24/02/2023

Acceptance date: 08/02/2023

Date deposited: 18/10/2024

ISSN (electronic): 2041-1723

Publisher: Nature Publishing Group

URL: https://doi.org/10.1038/s41467-023-36610-0

DOI: 10.1038/s41467-023-36610-0

Data Access Statement: The authors declare that the main data supporting the findings of this study are available within the paper and related Supplementary Information, Supplementary Data and Source Data files. Accession numbers to retrieve metagenomes analysed in this study are reported in Supplementary Table S3, Supplementary Data S3 and Supplementary Data S4 files. The mass spectrometry proteomics data are available via ProteomeXchange with identifier PXD039714. The data related to Tp have been deposited at researchdata.hhu.de under the identifier [https://doi.org/10.25838/d5p-42] 101. To use the archive, download the file, remove the .txt ending, and use WinRAR, for example, to open the archive. Microbiome sequences extracted from temperature variability sediments and related enriched heterotrophic bacteria were deposited in the NCBI database under the SRA accession number PRJNA508596. Source data are provided with this paper.


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Funding

Funder referenceFunder name
2020AEP061
FuturEnzyme Project funded by the European Union’s Horizon 2020 Research and Innovation Programme under Grant Agreement No. 101000327
German Federal Ministry of Education and Research (BMBF) through funding number 031B0837A “LipoBiocat”
Natural Environment Research Council UK (NERC), Grant No. NE/S004548/N
PID2020-112758RB-I00
PDC2021-121534-I00
Spanish National Center for Biotechnology, ProteoRed, PRB3-ISCIII.
uropean Regional Development Fund (EFRE) through funding no. 34-EFRE-0300096 “CLIB-Kompetenzzentrum Biotechnologie (CKB)”
TED2021-130544B-I00

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