TY - JOUR

T1 - Enzyme adaptation to habitat thermal legacy shapes the thermal plasticity of marine microbiomes

AU - Marasco, Ramona

AU - Fusi, Marco

AU - Coscolín, Cristina

AU - Borozzi, Alan

AU - Almendral, David

AU - Bargiela, Rafael

AU - Gohlke neé Nutschel, Christina

AU - Dittrich, Jonas

AU - Gohlke, Holger

AU - Matesanz, Ruth

AU - Sanchez-Carrillo, Sergio

AU - Mapelli, Francesca

AU - Chernikova, Tatyana

AU - Golyshin, Peter

AU - Ferrer, Manuel

AU - Daffonchio, Daniele

N1 - © 2023. The Author(s).

PY - 2023/2/24

Y1 - 2023/2/24

N2 - 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.

AB - 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.

KW - Cellular microbiology

KW - Ecophysiology

KW - Marine biology

KW - Microbial ecology

KW - Water Microbiology

U2 - 10.1038/s41467-023-36610-0

DO - 10.1038/s41467-023-36610-0

M3 - Article

C2 - 36828822

VL - 14

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 1045

ER -