Signatures of optimal codon usage in metabolic genes inform budding yeast ecology.
Carbohydrate Metabolism
/ genetics
Codon
Codon Usage
/ physiology
Ecosystem
Galactose
/ metabolism
Gene-Environment Interaction
Genes, Fungal
/ physiology
Genetic Association Studies
Metabolic Networks and Pathways
/ genetics
Organisms, Genetically Modified
Saccharomyces cerevisiae
/ genetics
Saccharomycetales
/ classification
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
22
07
2020
accepted:
15
03
2021
revised:
29
04
2021
pubmed:
20
4
2021
medline:
25
8
2021
entrez:
19
4
2021
Statut:
epublish
Résumé
Reverse ecology is the inference of ecological information from patterns of genomic variation. One rich, heretofore underutilized, source of ecologically relevant genomic information is codon optimality or adaptation. Bias toward codons that match the tRNA pool is robustly associated with high gene expression in diverse organisms, suggesting that codon optimization could be used in a reverse ecology framework to identify highly expressed, ecologically relevant genes. To test this hypothesis, we examined the relationship between optimal codon usage in the classic galactose metabolism (GAL) pathway and known ecological niches for 329 species of budding yeasts, a diverse subphylum of fungi. We find that optimal codon usage in the GAL pathway is positively correlated with quantitative growth on galactose, suggesting that GAL codon optimization reflects increased capacity to grow on galactose. Optimal codon usage in the GAL pathway is also positively correlated with human-associated ecological niches in yeasts of the CUG-Ser1 clade and with dairy-associated ecological niches in the family Saccharomycetaceae. For example, optimal codon usage of GAL genes is greater than 85% of all genes in the genome of the major human pathogen Candida albicans (CUG-Ser1 clade) and greater than 75% of genes in the genome of the dairy yeast Kluyveromyces lactis (family Saccharomycetaceae). We further find a correlation between optimization in the GALactose pathway genes and several genes associated with nutrient sensing and metabolism. This work suggests that codon optimization harbors information about the metabolic ecology of microbial eukaryotes. This information may be particularly useful for studying fungal dark matter-species that have yet to be cultured in the lab or have only been identified by genomic material.
Identifiants
pubmed: 33872297
doi: 10.1371/journal.pbio.3001185
pii: PBIOLOGY-D-20-02210
pmc: PMC8084343
doi:
Substances chimiques
Codon
0
Galactose
X2RN3Q8DNE
Banques de données
figshare
['10.6084/m9.figshare.c.4498292', '10.6084/m9.figshare.c.5067962']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3001185Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
J Biol Chem. 1949 May;179(1):497
pubmed: 18119268
Mol Biol Cell. 2016 Nov 1;27(21):3369-3375
pubmed: 27630263
Ann Intern Med. 1979 Oct;91(4):539-43
pubmed: 384857
Mol Cell Biol. 1992 Jul;12(7):2924-30
pubmed: 1377774
Nature. 2007 Oct 11;449(7163):677-81
pubmed: 17928853
Cell. 2016 Sep 22;167(1):122-132.e9
pubmed: 27641505
Elife. 2017 Feb 03;6:
pubmed: 28157073
Nucleic Acids Res. 1982 Nov 25;10(22):7055-74
pubmed: 6760125
PLoS Genet. 2016 Oct 14;12(10):e1006372
pubmed: 27741250
Nature. 2016 Feb 18;530(7590):336-9
pubmed: 26863195
Mol Biol Evol. 2018 Aug 1;35(8):1968-1981
pubmed: 29788479
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):10136-41
pubmed: 20479238
Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3645-50
pubmed: 20133581
Genetics. 1964 May;49:837-44
pubmed: 14158615
Elife. 2016 Sep 30;5:
pubmed: 27690225
Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9721-6
pubmed: 10449761
PLoS Genet. 2019 Jul 31;15(7):e1008304
pubmed: 31365533
Proc Natl Acad Sci U S A. 2004 Sep 28;101(39):14144-9
pubmed: 15381776
Int J Food Microbiol. 2006 Apr 15;108(1):130-5
pubmed: 16380183
FEMS Yeast Res. 2016 Jun;16(4):
pubmed: 27188884
Yeast. 2017 Jan;34(1):3-17
pubmed: 27668700
Science. 2002 Sep 27;297(5590):2253-6
pubmed: 12351787
Int Rev Cell Mol Biol. 2008;269:111-50
pubmed: 18779058
Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482-7
pubmed: 10200288
J Mol Biol. 1981 Feb 15;146(1):1-21
pubmed: 6167728
FEMS Microbiol Rev. 2014 Mar;38(2):254-99
pubmed: 24483210
J Theor Biol. 2002 Sep 21;218(2):175-85
pubmed: 12381290
Proc Natl Acad Sci U S A. 1988 Jun;85(12):4242-6
pubmed: 3288988
Sci Rep. 2015 Oct 20;5:15147
pubmed: 26482106
Heredity (Edinb). 2005 Feb;94(2):217-28
pubmed: 15523507
Genetics. 1991 Nov;129(3):897-907
pubmed: 1752426
Curr Biol. 2009 Mar 10;19(5):436-41
pubmed: 19249212
Bioinformatics. 2019 Feb 1;35(3):526-528
pubmed: 30016406
Science. 2008 Oct 10;322(5899):255-7
pubmed: 18755942
Genome Biol Evol. 2019 Apr 1;11(4):1054-1065
pubmed: 30859203
Oncogene. 2011 Apr 14;30(15):1841-9
pubmed: 21151172
Evolution. 2008 Dec;62(12):2984-94
pubmed: 18752601
Curr Opin Biotechnol. 2018 Feb;49:199-206
pubmed: 29102814
Fungal Genet Biol. 2007 Jun;44(6):563-74
pubmed: 17178245
BMC Evol Biol. 2011 Sep 28;11:279
pubmed: 21955875
Bioresour Technol. 2009 Aug;100(15):3734-9
pubmed: 19254836
Genes Cells. 2009 Apr;14(4):499-509
pubmed: 19335619
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
PLoS Genet. 2009 Jul;5(7):e1000556
pubmed: 19593368
Nature. 2013 Jul 25;499(7459):431-7
pubmed: 23851394
Mol Biol Evol. 1987 May;4(3):222-30
pubmed: 3328816
Biotechnol Bioeng. 2008 Oct 1;101(2):317-26
pubmed: 18421797
Res Microbiol. 2010 Jul-Aug;161(6):480-7
pubmed: 20302928
Cell. 2015 Mar 12;160(6):1111-24
pubmed: 25768907
Mol Biol Evol. 2002 Jan;19(1):110-7
pubmed: 11752196
Nature. 2010 Mar 4;464(7285):54-8
pubmed: 20164837
Bioinformatics. 2003 Oct;19 Suppl 2:ii215-25
pubmed: 14534192
Bioinformatics. 2019 Sep 15;35(18):3224-3231
pubmed: 30689741
Adv Exp Med Biol. 2012;751:329-45
pubmed: 22821465
Nature. 2006 Aug 3;442(7102):563-7
pubmed: 16885984
Eukaryot Cell. 2010 Jul;9(7):1075-86
pubmed: 20435697
Nature. 1997 Jun 12;387(6634):708-13
pubmed: 9192896
EMBO J. 1998 May 1;17(9):2566-73
pubmed: 9564039
Nat Rev Genet. 2013 Nov;14(11):807-20
pubmed: 24136507
Sci Rep. 2016 May 06;6:25536
pubmed: 27150248
Microb Biotechnol. 2009 Mar;2(2):154-6
pubmed: 21261909
Med Mycol. 2007 Mar;45(2):97-121
pubmed: 17365647
Mol Biol Evol. 2012 Dec;29(12):3669-83
pubmed: 22740635
PLoS One. 2013;8(1):e54403
pubmed: 23326606
Genetics. 2013 Sep;195(1):275-87
pubmed: 23852385
PLoS Biol. 2007 Sep;5(9):e219
pubmed: 17696646
J Basic Microbiol. 2002;42(3):207-27
pubmed: 12111748
Nucleic Acids Res. 2016 Jan 4;44(D1):D457-62
pubmed: 26476454
PLoS Pathog. 2013;9(9):e1003550
pubmed: 24086128
Mol Gen Genet. 1983;191(1):31-8
pubmed: 6350827
PLoS Genet. 2014 Jun 05;10(6):e1004392
pubmed: 24901308
Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):2977-82
pubmed: 20133628
Bioinformatics. 2012 Mar 1;28(5):734-5
pubmed: 22219204
Comput Appl Biosci. 1997 Oct;13(5):555-6
pubmed: 9367129
Genome Res. 2004 Nov;14(11):2279-86
pubmed: 15479947
Proc Natl Acad Sci U S A. 1981 Sep;78(9):5739-43
pubmed: 6795634
Proc Natl Acad Sci U S A. 2011 May 3;108(18):7493-8
pubmed: 21498688
Food Microbiol. 2006 Jun;23(4):341-50
pubmed: 16943023
Nucleic Acids Res. 2013 Oct;41(19):8842-52
pubmed: 23921637
Int J Food Microbiol. 2001 Sep 19;69(1-2):37-44
pubmed: 11589558
Genomics. 2020 Jul;112(4):2695-2702
pubmed: 32145379
Proc Natl Acad Sci U S A. 2008 Sep 23;105(38):14482-7
pubmed: 18787117
FEMS Yeast Res. 2009 Dec;9(8):1338-42
pubmed: 19840117
Nat Rev Microbiol. 2016 Feb;14(2):106-17
pubmed: 26685750
Curr Biol. 2007 Jun 19;17(12):1007-13
pubmed: 17540568
J Clin Microbiol. 2009 Jan;47(1):242-4
pubmed: 19036938
Gut Microbes. 2014 Mar-Apr;5(2):265-70
pubmed: 24637600
PLoS One. 2018 May 9;13(5):e0195869
pubmed: 29742107
J Econ Entomol. 1946 Apr;39:269
pubmed: 20983181
Elife. 2016 Sep 10;5:
pubmed: 27614020
Genomics Inform. 2017 Mar;15(1):38-47
pubmed: 28416948
J Biosci Bioeng. 2011 Feb;111(2):158-66
pubmed: 21075050
Science. 2004 Sep 3;305(5689):1462-5
pubmed: 15353802
Mol Biol Evol. 2007 Feb;24(2):374-81
pubmed: 17101719
Lett Appl Microbiol. 2011 Nov;53(5):503-8
pubmed: 21801184
Cell. 2019 Mar 7;176(6):1356-1366.e10
pubmed: 30799038
BMC Bioinformatics. 2016 Jul 29;17(1):294
pubmed: 27473172
Food Microbiol. 2014 Apr;38:171-8
pubmed: 24290641
DNA Res. 2009 Feb;16(1):13-30
pubmed: 19131380
Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):2831-6
pubmed: 21282627
Cell. 2018 Nov 29;175(6):1533-1545.e20
pubmed: 30415838
Genetics. 2021 Feb 9;217(2):
pubmed: 33724406
Elife. 2020 Jan 28;9:
pubmed: 31989922
FEMS Yeast Res. 2019 May 1;19(3):
pubmed: 31076749
Trends Genet. 2017 Apr;33(4):283-297
pubmed: 28292534
Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):E6117-E6125
pubmed: 27671647
Bioinformatics. 2017 Feb 15;33(4):589-591
pubmed: 27797757
J Clin Microbiol. 1990 Oct;28(10):2224-7
pubmed: 2229346
Proc Natl Acad Sci U S A. 2016 Aug 30;113(35):9882-7
pubmed: 27535936
Curr Opin Microbiol. 2005 Aug;8(4):385-92
pubmed: 16019255
BMC Biol. 2018 Mar 2;16(1):26
pubmed: 29499717
Cell Microbiol. 2010 Jul;12(7):863-72
pubmed: 20482553
Gene X. 2019 Mar 06;2:100012
pubmed: 32550546
Nat Rev Genet. 2008 Aug;9(8):583-93
pubmed: 18591982
Int J Food Microbiol. 2017 Jan 16;241:191-197
pubmed: 27794247
Am Nat. 2000 Mar;155(3):346-364
pubmed: 10718731
Syst Biol. 2012 May;61(3):382-91
pubmed: 22215720
Genome Biol. 2004;5(4):R26
pubmed: 15059259
Nucleic Acids Res. 2010 Jul;38(Web Server issue):W7-13
pubmed: 20435676