Evolution of Linoleic Acid Biosynthesis Paved the Way for Ecological Success of Termites.

Blattodea Isoptera biosynthesis fatty acyl desaturases linoleic acid termites

Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
04 04 2023
Historique:
medline: 1 5 2023
pubmed: 13 4 2023
entrez: 12 4 2023
Statut: ppublish

Résumé

Termites are dominant animals of tropical terrestrial ecosystems. Their success is due to their eusocial organization as well as their ability to digest dead plant tissues. While being extremely abundant, the termite diet is poor in crucial nutrients, such as fatty acids. Linoleic acid (LA) is a precursor for many vital biomolecules, and most animals depend on its dietary supply. Termites count among the exceptions known to produce LA de novo, presumably via the action of an unknown Δ12 fatty acyl desaturase (FAD) introducing the second double bond into monounsaturated oleic acid. Here, we search for the evolutionary origin of LA biosynthesis in termites. To this end, we compile the repertoire of FAD homologs from 57 species of termites and their closest relatives, the cockroaches, analyze FAD phylogeny, and identify a potential Δ12 FAD branch, which arose through duplication of a likely Δ9 FAD. We functionally characterize both paralogs and identify the Δ9 activity in the ancestral FAD-A1a and the Δ12 activity responsible for LA biosynthesis in FAD-A1b. Through the combination of homology modeling and site-directed mutagenesis, we pinpoint structural features possibly contributing to the distinct functions, regiospecificities, and substrate preferences of the two enzymes. We confirm the presence of both paralogs in all 36 studied species of the Blattoidea lineage (Blattidae, Lamproblattidae, Cryptocercidae, and termites) and conclude that we identified an evolutionary event important for the ecological success of termites, which took place in their cockroach ancestors roughly 160 My and remained conserved throughout termite diversification into 3,000 extant species.

Identifiants

pubmed: 37043525
pii: 7116159
doi: 10.1093/molbev/msad087
pmc: PMC10139705
pii:
doi:

Substances chimiques

Linoleic Acid 9KJL21T0QJ
Fatty Acids 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

Références

Micron. 2006;37(7):648-56
pubmed: 16632370
Nat Methods. 2022 Jun;19(6):679-682
pubmed: 35637307
Arch Biochem Biophys. 1968 Jul;126(1):131-40
pubmed: 5671057
Nature. 2015 Aug 13;524(7564):252-6
pubmed: 26098370
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Nat Struct Mol Biol. 2015 Jul;22(7):581-5
pubmed: 26098317
Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8631-6
pubmed: 15173596
J Chem Ecol. 2016 Oct;42(10):1070-1081
pubmed: 27639394
Evol Biol. 2018;45(1):15-26
pubmed: 29497218
Insect Biochem Mol Biol. 2011 Sep;41(9):715-22
pubmed: 21651981
Nat Rev Microbiol. 2014 Mar;12(3):168-80
pubmed: 24487819
Proc Biol Sci. 2021 Apr 28;288(1949):20210511
pubmed: 33878922
Insect Biochem Mol Biol. 1999 Jun;29(6):481-514
pubmed: 10406089
Nat Ecol Evol. 2018 Mar;2(3):557-566
pubmed: 29403074
Insect Biochem Mol Biol. 2013 Aug;43(8):724-31
pubmed: 23727612
Mol Biol Evol. 2015 Feb;32(2):456-71
pubmed: 25425561
J Chem Ecol. 1985 Mar;11(3):265-77
pubmed: 24309959
Trends Ecol Evol. 2008 Apr;23(4):220-8
pubmed: 18308422
Insect Biochem Mol Biol. 2013 Nov;43(11):991-6
pubmed: 23973745
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
J Chem Ecol. 1992 Mar;18(3):517-26
pubmed: 24254954
Appl Environ Microbiol. 1983 May;45(5):1602-13
pubmed: 16346296
Nature. 2010 Jul 22;466(7305):486-9
pubmed: 20592730
J Mol Biol. 2020 Aug 21;432(18):5152-5161
pubmed: 32470559
Nature. 1973 Aug 31;244(5418):577-80
pubmed: 4582514
Mol Biol Evol. 2009 Jul;26(7):1447-56
pubmed: 19307313
Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9449-54
pubmed: 10920187
Genetics. 2002 Dec;162(4):1737-52
pubmed: 12524345
Chem Pharm Bull (Tokyo). 2019;67(4):327-332
pubmed: 30930436
Science. 1961 Jul 7;134(3471):50
pubmed: 17834302
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9179-84
pubmed: 12876197
Curr Biol. 2019 Nov 4;29(21):3728-3734.e4
pubmed: 31630948
Insect Biochem Mol Biol. 2014 Feb;45:51-7
pubmed: 24333472
Proc Natl Acad Sci U S A. 2010 Jun 15;107(24):10955-60
pubmed: 20534481
Proc Biol Sci. 2019 Jan 30;286(1895):20182076
pubmed: 30963947
Biol Rev Camb Philos Soc. 2020 Jun;95(3):555-572
pubmed: 31876057
ACS Chem Biol. 2014 Apr 18;9(4):922-34
pubmed: 24475735
Proc Natl Acad Sci U S A. 2007 Oct 16;104(42):16444-9
pubmed: 17921252
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6
pubmed: 23193283
Nat Commun. 2012;3:1150
pubmed: 23093187
Annu Rev Entomol. 2016;61:99-117
pubmed: 26565898
J Chem Ecol. 1990 Aug;16(8):2549-57
pubmed: 24264219
Protein Sci. 2021 Jan;30(1):70-82
pubmed: 32881101
Protein Expr Purif. 2002 Aug;25(3):372-8
pubmed: 12182816
Insect Biochem Mol Biol. 2010 Oct;40(10):742-51
pubmed: 20691782
J Biol Chem. 2020 Aug 7;295(32):11337-11345
pubmed: 32527722
Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12586-91
pubmed: 26417103
Insect Biochem Mol Biol. 2008 Feb;38(2):244-55
pubmed: 18207084
J Bacteriol. 2000 Jul;182(13):3655-60
pubmed: 10850979
Nat Commun. 2014 May 20;5:3636
pubmed: 24845553
Prostaglandins Leukot Essent Fatty Acids. 2003 Feb;68(2):73-95
pubmed: 12538072
Insect Mol Biol. 2008 Dec;17(6):667-76
pubmed: 19133076
J Biol Chem. 2011 Apr 15;286(15):12860-9
pubmed: 21300802
Comput Struct Biotechnol J. 2020 May 14;18:1202-1209
pubmed: 32542106
Mol Biol Evol. 2018 Feb 1;35(2):518-522
pubmed: 29077904
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Nature. 1968 Aug 31;219(5157):963-4
pubmed: 5673020
Z Naturforsch C J Biosci. 2017 Sep 26;72(9-10):387-403
pubmed: 28742527
J Exp Biol. 2019 May 16;222(Pt 10):
pubmed: 31019064
Mol Phylogenet Evol. 2017 Oct;115:50-57
pubmed: 28739372
Elife. 2019 Feb 04;8:
pubmed: 30714899
J Lipid Res. 2015 Dec;56(12):2309-21
pubmed: 26486975
Insect Biochem Mol Biol. 2007 Jun;37(6):601-10
pubmed: 17517337
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Insect Biochem Mol Biol. 2016 Jul;74:68-75
pubmed: 27163509
Gigascience. 2015 Oct 19;4:48
pubmed: 26500767
Mol Biol Evol. 2010 Feb;27(2):221-4
pubmed: 19854763
Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:611-641
pubmed: 15012248

Auteurs

Stanislav Macháček (S)

Viral and Microbial Proteins, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.
Department of Biochemistry and Microbiology, University of Chemistry and Technology Prague, Prague, Czech Republic.

Michal Tupec (M)

Viral and Microbial Proteins, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.
Faculty of Science, Charles University, Prague, Czech Republic.

Natan Horáček (N)

Faculty of Science, Charles University, Prague, Czech Republic.
Chemistry of Social Insects, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.

Martina Halmová (M)

Viral and Microbial Proteins, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.
Faculty of Science, Charles University, Prague, Czech Republic.

Amit Roy (A)

Forest Molecular Entomology Lab, Czech University of Life Sciences, Prague, Czech Republic.

Aleš Machara (A)

Drug Discovery, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.

Pavlína Kyjaková (P)

Chemistry of Social Insects, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.

Ondřej Lukšan (O)

Chemistry of Social Insects, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.

Iva Pichová (I)

Viral and Microbial Proteins, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.

Robert Hanus (R)

Chemistry of Social Insects, Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH