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


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
24 02 2023
Historique:
received: 25 12 2021
accepted: 08 02 2023
entrez: 24 2 2023
pubmed: 25 2 2023
medline: 3 3 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 36828822
doi: 10.1038/s41467-023-36610-0
pii: 10.1038/s41467-023-36610-0
pmc: PMC9958047
doi:

Substances chimiques

Esterases EC 3.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1045

Informations de copyright

© 2023. The Author(s).

Références

CSH Protoc. 2006 Jun 01;2006(1):
pubmed: 22485641
J Phys Chem B. 2008 Jul 31;112(30):9020-41
pubmed: 18593145
PLoS Comput Biol. 2012;8(10):e1002708
pubmed: 23093919
Nat Methods. 2015 Jan;12(1):59-60
pubmed: 25402007
Microb Biotechnol. 2016 Jan;9(1):22-34
pubmed: 26275154
J Mol Biol. 1999 Jan 29;285(4):1735-47
pubmed: 9917408
Front Microbiol. 2013 Nov 12;4:333
pubmed: 24339821
Appl Microbiol Biotechnol. 2015 Dec;99(23):10031-46
pubmed: 26266751
Nucleic Acids Res. 2013 Jan 7;41(1):e1
pubmed: 22933715
PLoS Comput Biol. 2016 Mar 22;12(3):e1004754
pubmed: 27003415
J Chem Inf Model. 2021 May 24;61(5):2383-2395
pubmed: 33949194
Arch Microbiol. 2022 Jan 19;204(2):144
pubmed: 35044532
J Comput Chem. 2005 Dec;26(16):1668-88
pubmed: 16200636
Biophys J. 2013 Aug 6;105(3):783-93
pubmed: 23931326
J Biotechnol. 2012 Jun 15;159(3):135-44
pubmed: 22326626
Nucleic Acids Res. 2013 Jul;41(Web Server issue):W340-8
pubmed: 23609541
J Exp Biol. 2020 Oct 8;223(Pt 19):
pubmed: 32778564
Nat Commun. 2019 Mar 21;10(1):1314
pubmed: 30899017
Ann Rev Mar Sci. 2012;4:39-61
pubmed: 22457968
Environ Microbiol. 2015 Jul;17(7):2421-9
pubmed: 25403257
Ecol Lett. 2015 Jan;18(1):85-95
pubmed: 25430889
Nat Ecol Evol. 2019 Feb;3(2):223-231
pubmed: 30643243
Nat Rev Microbiol. 2015 Mar;13(3):133-46
pubmed: 25659323
Proteins. 2001 Aug 1;44(2):150-65
pubmed: 11391777
Philos Trans R Soc Lond B Biol Sci. 2020 Dec 21;375(1814):20190454
pubmed: 33131443
Proc Natl Acad Sci U S A. 2016 May 17;113(20):5700-5
pubmed: 27140608
J Chem Theory Comput. 2015 Apr 14;11(4):1864-74
pubmed: 26574392
Nat Methods. 2022 Jun;19(6):679-682
pubmed: 35637307
Appl Environ Microbiol. 2019 Jan 9;85(2):
pubmed: 30413473
J Chem Theory Comput. 2015 Aug 11;11(8):3696-713
pubmed: 26574453
Nat Rev Microbiol. 2003 Dec;1(3):200-8
pubmed: 15035024
Annu Rev Physiol. 1995;57:43-68
pubmed: 7778874
Nat Rev Microbiol. 2019 Jun;17(6):391-396
pubmed: 31092905
Glob Chang Biol. 2020 Jan;26(1):54-67
pubmed: 31743515
Nature. 2007 Aug 2;448(7153):550-2
pubmed: 17671497
Science. 2013 Jun 28;340(6140):1574-7
pubmed: 23812714
J Chem Theory Comput. 2013 Sep 10;9(9):3878-88
pubmed: 26592383
Glob Ecol Biogeogr. 2021 May;30(5):987-999
pubmed: 33867861
J Chem Inf Model. 2013 Apr 22;53(4):1007-15
pubmed: 23517329
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Appl Environ Microbiol. 1990 Mar;56(3):595-600
pubmed: 16348135
Philos Trans R Soc Lond B Biol Sci. 2019 Aug 5;374(1778):20180549
pubmed: 31203764
J Chem Inf Model. 2020 Mar 23;60(3):1568-1584
pubmed: 31905288
J Comput Chem. 2013 Jan 30;34(3):220-33
pubmed: 23007873
PLoS One. 2013 Jun 05;8(6):e64909
pubmed: 23755161
Phys Biol. 2005 Nov 09;2(4):S137-47
pubmed: 16280619
Science. 2017 Sep 15;357(6356):
pubmed: 28912213
J Microbiol Methods. 2000 Aug;41(3):249-57
pubmed: 10958970
FEBS J. 2020 Mar;287(5):1035-1053
pubmed: 31545554
J Exp Biol. 2010 Mar 15;213(6):881-93
pubmed: 20190113
Nucleic Acids Res. 2019 Jan 8;47(D1):D442-D450
pubmed: 30395289
Nat Microbiol. 2020 Nov;5(11):1428-1438
pubmed: 32807893
Science. 2008 Oct 31;322(5902):690-2
pubmed: 18974339
Front Microbiol. 2019 Feb 28;10:331
pubmed: 30873139
PLoS One. 2015 Jul 06;10(7):e0130289
pubmed: 26147762
Nat Commun. 2023 Feb 24;14(1):1045
pubmed: 36828822
Sci Adv. 2019 Sep 04;5(9):eaax1814
pubmed: 31517051
Ann Rev Mar Sci. 2013;5:371-92
pubmed: 22809195
Adv Protein Chem. 1988;39:191-234
pubmed: 3072868
Philos Trans R Soc Lond B Biol Sci. 2019 Mar 18;374(1768):20180174
pubmed: 30966962
Sci Rep. 2017 Aug 15;7(1):8144
pubmed: 28811521
Nat Commun. 2013;4:2156
pubmed: 23877221
Trends Microbiol. 2017 Jun;25(6):494-505
pubmed: 28108182
Nat Ecol Evol. 2017 Sep;1(9):1339-1347
pubmed: 29046544
Mol Ecol. 2014 Feb;23(4):954-64
pubmed: 24460915
PLoS One. 2016 Nov 9;11(11):e0163939
pubmed: 27828965
Appl Environ Microbiol. 2015 Mar;81(6):2125-36
pubmed: 25595762
Nat Methods. 2010 May;7(5):335-6
pubmed: 20383131
Science. 2015 May 22;348(6237):1261359
pubmed: 25999513
Proc Natl Acad Sci U S A. 2022 Mar 15;119(11):e2111332119
pubmed: 35254906
Nature. 2018 Aug;560(7718):299-301
pubmed: 30108353
Nat Commun. 2020 Feb 6;11(1):754
pubmed: 32029713
Appl Environ Microbiol. 2020 Nov 24;86(24):
pubmed: 32978141
J Exp Biol. 2010 Mar 15;213(6):912-20
pubmed: 20190116
Glob Chang Biol. 2018 Sep;24(9):4330-4339
pubmed: 29750385
Sci Rep. 2016 Jan 19;6:17908
pubmed: 26783049
Appl Environ Microbiol. 2016 Apr 04;82(8):2467-2478
pubmed: 26896130
ACS Chem Biol. 2018 Jan 19;13(1):225-234
pubmed: 29182315
Aging Cell. 2020 Jan;19(1):e13063
pubmed: 31730262
Front Microbiol. 2017 Aug 22;8:1599
pubmed: 28878754
Nat Ecol Evol. 2019 Feb;3(2):232-238
pubmed: 30643242
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12917-22
pubmed: 12235364
IEEE/ACM Trans Comput Biol Bioinform. 2016 May-Jun;13(3):505-17
pubmed: 27295634
Proteins. 2011 Apr;79(4):1089-108
pubmed: 21246632
Int J Mol Sci. 2017 Dec 11;18(12):
pubmed: 29232922
Science. 2007 Jan 26;315(5811):513-5
pubmed: 17255511
Nature. 2011 Feb 24;470(7335):479-85
pubmed: 21350480
J Exp Biol. 2016 Mar;219(Pt 5):686-94
pubmed: 26747904
Protein Sci. 1997 Jun;6(6):1333-7
pubmed: 9194194

Auteurs

Ramona Marasco (R)

Biological and Environmental Sciences and Engineering Division (BESE), Red Sea Research Centre (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Marco Fusi (M)

Biological and Environmental Sciences and Engineering Division (BESE), Red Sea Research Centre (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.
Centre for Conservation and Restoration Science, Edinburgh Napier University Sighthill Campus, Edinburgh, UK.

Cristina Coscolín (C)

Instituto de Catalisis y Petroleoquimica (ICP), CSIC, Madrid, Spain.

Alan Barozzi (A)

Biological and Environmental Sciences and Engineering Division (BESE), Red Sea Research Centre (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

David Almendral (D)

Instituto de Catalisis y Petroleoquimica (ICP), CSIC, Madrid, Spain.

Rafael Bargiela (R)

Centre for Environmental Biotechnology, School of Natural Sciences, Bangor University, Deiniol Rd, Bangor, UK.

Christina Gohlke Neé Nutschel (CGN)

Institute of Bio- and Geosciences (IBG-4: Bioinformatics), Forschungszentrum Jülich GmbH, Jülich, Germany.

Christopher Pfleger (C)

Mathematisch-Naturwissenschaftliche Fakultät, Institut für Pharmazeutische und Medizinische Chemie, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany.

Jonas Dittrich (J)

Mathematisch-Naturwissenschaftliche Fakultät, Institut für Pharmazeutische und Medizinische Chemie, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany.

Holger Gohlke (H)

Institute of Bio- and Geosciences (IBG-4: Bioinformatics), Forschungszentrum Jülich GmbH, Jülich, Germany.
Mathematisch-Naturwissenschaftliche Fakultät, Institut für Pharmazeutische und Medizinische Chemie, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany.
John von Neumann Institute for Computing (NIC) and Jülich Supercomputing Centre (JSC), Forschungszentrum Jülich GmbH, Jülich, Germany.

Ruth Matesanz (R)

Spectroscopy Laboratory, Centro de Investigaciones Biologicas Margarita Salas (CIB), CSIC, Madrid, Spain.

Sergio Sanchez-Carrillo (S)

Instituto de Catalisis y Petroleoquimica (ICP), CSIC, Madrid, Spain.
Centro de Biologia Molecular Severo Ochoa (CBM), CSIC-UAM, Madrid, Spain.

Francesca Mapelli (F)

Department of Food Environmental and Nutritional Sciences, University of Milan, Milan, Italy.

Tatyana N Chernikova (TN)

Centre for Environmental Biotechnology, School of Natural Sciences, Bangor University, Deiniol Rd, Bangor, UK.

Peter N Golyshin (PN)

Centre for Environmental Biotechnology, School of Natural Sciences, Bangor University, Deiniol Rd, Bangor, UK.

Manuel Ferrer (M)

Instituto de Catalisis y Petroleoquimica (ICP), CSIC, Madrid, Spain. mferrer@icp.csic.es.

Daniele Daffonchio (D)

Biological and Environmental Sciences and Engineering Division (BESE), Red Sea Research Centre (RSRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia. daniele.daffonchio@kaust.edu.sa.

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