Codon Optimization Improves the Prediction of Xylose Metabolism from Gene Content in Budding Yeasts

Xylose is the second most abundant monomeric sugar in plant biomass. Consequently, xylose catabolism is an ecologically important trait for saprotrophic organisms, as well as a fundamentally important trait for industries that hope to convert plant mass to renewable fuels and other bioproducts using...

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Bibliographic Details
Published in:Molecular biology and evolution 2023-06, Vol.40 (6)
Main Authors: Nalabothu, Rishitha L, Fisher, Kaitlin J, LaBella, Abigail Leavitt, Meyer, Taylor A, Opulente, Dana A, Wolters, John F, Rokas, Antonis, Hittinger, Chris Todd
Format: Article
Language:English
Subjects:
BASIC BIOLOGICAL SCIENCES
Biological products
Codon
codon optimization
Discoveries
Fermentation
Genes
genome evolution
Genomes
Genomics
metabolic evolution
Monosaccharides
Phylogeny
Sugars
yeasts
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Summary:Xylose is the second most abundant monomeric sugar in plant biomass. Consequently, xylose catabolism is an ecologically important trait for saprotrophic organisms, as well as a fundamentally important trait for industries that hope to convert plant mass to renewable fuels and other bioproducts using microbial metabolism. Although common across fungi, xylose catabolism is rare within Saccharomycotina, the subphylum that contains most industrially relevant fermentative yeast species. The genomes of several yeasts unable to consume xylose have been previously reported to contain the full set of genes in the XYL pathway, suggesting the absence of a gene-trait correlation for xylose metabolism. Here, we measured growth on xylose and systematically identified XYL pathway orthologs across the genomes of 332 budding yeast species. Although the XYL pathway coevolved with xylose metabolism, we found that pathway presence only predicted xylose catabolism about half of the time, demonstrating that a complete XYL pathway is necessary, but not sufficient, for xylose catabolism. We also found that XYL1 copy number was positively correlated, after phylogenetic correction, with xylose utilization. We then quantified codon usage bias of XYL genes and found that XYL3 codon optimization was significantly higher, after phylogenetic correction, in species able to consume xylose. Finally, we showed that codon optimization of XYL2 was positively correlated, after phylogenetic correction, with growth rates in xylose medium. We conclude that gene content alone is a weak predictor of xylose metabolism and that using codon optimization enhances the prediction of xylose metabolism from yeast genome sequence data.
ISSN:0737-4038
1537-1719
DOI:10.1093/molbev/msad111