Global Shifts in Genome and Proteome Composition Are Very Tightly Coupled

Brbić, Maria; Warnecke, Tobias; Kriško, Anita; Supek, Fran (2015) Global Shifts in Genome and Proteome Composition Are Very Tightly Coupled. Genome Biology and Evolution, 7 (6). pp. 1519-1532. ISSN 1759-6653

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Official URL: http://gbe.oxfordjournals.org/content/7/6/1519.ful...

Abstract

The amino acid composition (AAC) of proteomes differs greatly between microorganisms and is associated with the environmental niche they inhabit, suggesting that these changes may be adaptive. Similarly, the oligonucleotide composition of genomes varies and may confer advantages at the DNA/RNA level. These influences overlap in protein-coding sequences, making it difficult to gauge their relative contributions. We disentangle these effects by systematically evaluating the correspondence between intergenic nucleotide composition, where protein-level selection is absent, the AAC, and ecological parameters of 909 prokaryotes. We find that G + C content, the most frequently used measure of genomic composition, cannot capture diversity in AAC and across ecological contexts. However, di-/trinucleotide composition in intergenic DNA predicts amino acid frequencies of proteomes to the point where very little cross-species variability remains unexplained (91% of variance accounted for). Qualitatively similar results were obtained for 49 fungal genomes, where 80% of the variability in AAC could be explained by the composition of introns and intergenic regions. Upon factoring out oligonucleotide composition and phylogenetic inertia, the residual AAC is poorly predictive of the microbes’ ecological preferences, in stark contrast with the original AAC. Moreover, highly expressed genes do not exhibit more prominent environment-related AAC signatures than lowly expressed genes, despite contributing more to the effective proteome. Thus, evolutionary shifts in overall AAC appear to occur almost exclusively through factors shaping the global oligonucleotide content of the genome. We discuss these results in light of contravening evidence from biophysical data and further reading frame-specific analyses that suggest that adaptation takes place at the protein level.

Item Type:

Article

Additional Information:

This work was supported by the Mediterranean Institute for Life Sciences and Fondation Nelia et Amadeo Barletta (to M.B.and A.K.), by MRC core funding and an Imperial College Junior Research Fellowship (to T.W.), by FP7 FET grant ICT-2013-612944 MAESTRA (to F.S. and M.B.), by FP7 REGPOT grant InnoMol (to F.S.), by the Croatian Science Foundation grant HRZZ-9623 (to M.B.), and the Croatian Ministry of Science and Sport grant 098-0000000-3168 (to F.S.).

Uncontrolled Keywords:

amino acid composition, oligonucleotide composition, intergenic DNA, ecological preferences, prokaryotic genome, fungal genome, support vector regression

Subjects:

NATURAL SCIENCES > Biology > Genetics, Evolution and Phylogenetics
TECHNICAL SCIENCES > Computing > Artificial Intelligence

Divisions:

Division of Electronics

Projects:

Project title	Project leader	Project code	Project type
Strojno učenje prediktivnih modela u računalnoj biologiji	Tomislav Šmuc	098-0000000-3168	MZOS
Learning from Massive, Incompletely annotated, and Structured Data-MAESTRA	UNSPECIFIED	612944	EK
Enhancement of the Innovation Potential in SEE through new Molecular Solutions in Research and Development-INNOMOL	UNSPECIFIED	316289	EK
Postupci strojnog učenja za dubinsku analizu složenih struktura podataka-DescriptiveInduction	Dragan Gamberger	IP-11-2013-9623	HRZZ