The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement
To survive in cold environments, psychrophilic organisms produce enzymes endowed with high specific activity at low temperature. The structure of these enzymes is usually flexible and mostly thermolabile. In this work, we investigate the structural basis of cold adaptation of a GH42 β-galactosidase...
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Online Access: | http://hdl.handle.net/11581/452966 https://doi.org/10.1111/febs.15354 |
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ftuncamerinoiris:oai:pubblicazioni.unicam.it:11581/452966 2024-04-14T08:03:53+00:00 The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement Mangiagalli M. Lapi M. Maione S. Orlando M. Brocca S. Pesce A. Barbiroli A. Camilloni C. Pucciarelli S. Lotti M. Nardini M. Mangiagalli, M. Lapi, M. Maione, S. Orlando, M. Brocca, S. Pesce, A. Barbiroli, A. Camilloni, C. Pucciarelli, S. Lotti, M. Nardini, M. 2021 http://hdl.handle.net/11581/452966 https://doi.org/10.1111/febs.15354 eng eng info:eu-repo/semantics/altIdentifier/wos/WOS:000537698000001 volume:288 issue:2 firstpage:546 lastpage:565 numberofpages:20 journal:THE FEBS JOURNAL http://hdl.handle.net/11581/452966 doi:10.1111/febs.15354 info:eu-repo/semantics/altIdentifier/scopus/2-s2.0-85085919958 info:eu-repo/semantics/article 2021 ftuncamerinoiris https://doi.org/10.1111/febs.15354 2024-03-21T20:38:37Z To survive in cold environments, psychrophilic organisms produce enzymes endowed with high specific activity at low temperature. The structure of these enzymes is usually flexible and mostly thermolabile. In this work, we investigate the structural basis of cold adaptation of a GH42 β-galactosidase from the psychrophilic Marinomonas ef1. This enzyme couples cold activity with astonishing robustness for a psychrophilic protein, for it retains 23% of its highest activity at 5°C and it is stable for several days at 37°C and even 50°C. Phylogenetic analyses indicate a close relationship with thermophilic β-galactosidases, suggesting that the present-day enzyme evolved from a thermostable scaffold modeled by environmental selective pressure. The crystallographic structure reveals the overall similarity with GH42 enzymes, along with a hexameric arrangement (dimer of trimers) not found in psychrophilic, mesophilic, and thermophilic homologues. In the quaternary structure, protomers form a large central cavity, whose accessibility to the substrate is promoted by the dynamic behavior of surface loops, even at low temperature. A peculiar cooperative behavior of the enzyme is likely related to the increase of the internal cavity permeability triggered by heating. Overall, our results highlight a novel strategy of enzyme cold adaptation, based on the oligomerization state of the enzyme, which effectively challenges the paradigm of cold activity coupled with intrinsic thermolability. Database: Structural data are available in the Protein Data Bank database under the accession number 6Y2K. Article in Journal/Newspaper Antarc* Antarctic CAMPUS Pubblicazioni Scientifiche Unicam (Università di Camerino) Antarctic The FEBS Journal 288 2 546 565 |
institution |
Open Polar |
collection |
CAMPUS Pubblicazioni Scientifiche Unicam (Università di Camerino) |
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ftuncamerinoiris |
language |
English |
description |
To survive in cold environments, psychrophilic organisms produce enzymes endowed with high specific activity at low temperature. The structure of these enzymes is usually flexible and mostly thermolabile. In this work, we investigate the structural basis of cold adaptation of a GH42 β-galactosidase from the psychrophilic Marinomonas ef1. This enzyme couples cold activity with astonishing robustness for a psychrophilic protein, for it retains 23% of its highest activity at 5°C and it is stable for several days at 37°C and even 50°C. Phylogenetic analyses indicate a close relationship with thermophilic β-galactosidases, suggesting that the present-day enzyme evolved from a thermostable scaffold modeled by environmental selective pressure. The crystallographic structure reveals the overall similarity with GH42 enzymes, along with a hexameric arrangement (dimer of trimers) not found in psychrophilic, mesophilic, and thermophilic homologues. In the quaternary structure, protomers form a large central cavity, whose accessibility to the substrate is promoted by the dynamic behavior of surface loops, even at low temperature. A peculiar cooperative behavior of the enzyme is likely related to the increase of the internal cavity permeability triggered by heating. Overall, our results highlight a novel strategy of enzyme cold adaptation, based on the oligomerization state of the enzyme, which effectively challenges the paradigm of cold activity coupled with intrinsic thermolability. Database: Structural data are available in the Protein Data Bank database under the accession number 6Y2K. |
author2 |
Mangiagalli, M. Lapi, M. Maione, S. Orlando, M. Brocca, S. Pesce, A. Barbiroli, A. Camilloni, C. Pucciarelli, S. Lotti, M. Nardini, M. |
format |
Article in Journal/Newspaper |
author |
Mangiagalli M. Lapi M. Maione S. Orlando M. Brocca S. Pesce A. Barbiroli A. Camilloni C. Pucciarelli S. Lotti M. Nardini M. |
spellingShingle |
Mangiagalli M. Lapi M. Maione S. Orlando M. Brocca S. Pesce A. Barbiroli A. Camilloni C. Pucciarelli S. Lotti M. Nardini M. The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement |
author_facet |
Mangiagalli M. Lapi M. Maione S. Orlando M. Brocca S. Pesce A. Barbiroli A. Camilloni C. Pucciarelli S. Lotti M. Nardini M. |
author_sort |
Mangiagalli M. |
title |
The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement |
title_short |
The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement |
title_full |
The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement |
title_fullStr |
The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement |
title_full_unstemmed |
The co-existence of cold activity and thermal stability in an Antarctic GH42 β-galactosidase relies on its hexameric quaternary arrangement |
title_sort |
co-existence of cold activity and thermal stability in an antarctic gh42 β-galactosidase relies on its hexameric quaternary arrangement |
publishDate |
2021 |
url |
http://hdl.handle.net/11581/452966 https://doi.org/10.1111/febs.15354 |
geographic |
Antarctic |
geographic_facet |
Antarctic |
genre |
Antarc* Antarctic |
genre_facet |
Antarc* Antarctic |
op_relation |
info:eu-repo/semantics/altIdentifier/wos/WOS:000537698000001 volume:288 issue:2 firstpage:546 lastpage:565 numberofpages:20 journal:THE FEBS JOURNAL http://hdl.handle.net/11581/452966 doi:10.1111/febs.15354 info:eu-repo/semantics/altIdentifier/scopus/2-s2.0-85085919958 |
op_doi |
https://doi.org/10.1111/febs.15354 |
container_title |
The FEBS Journal |
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288 |
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2 |
container_start_page |
546 |
op_container_end_page |
565 |
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