Revisiting the Relationships Between Genomic G + C Content, RNA Secondary Structures, and Optimal Growth Temperature

Meyer, Michelle M.

doi:10.1007/s00239-020-09974-w

Cited by 22 publications

(14 citation statements)

References 79 publications

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“…This genomic trait has been widely studied, and its evolution has been proposed to be associated with numerous mutational and selective forces driven by genetic, metabolic, and ecological factors [ 4 – 19 ]. The high temperature might be the most long-debating [ 20 – 22 ]. Because G:C pairs have an additional hydrogen bond than A:T pairs, the GC-rich genomes are expected to be thermally more stable in high-temperature environments [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

“…Still, this study did not shake the confidence of Musto et al [ 35 ] on the correlation between Topt and genomic GC content in prokaryotes. Although Musto and coauthors have rebutted all the criticisms, their studies have not convinced later authors of review articles [ 4 , 20 , 36 ]. For example, Agashe and Shankar [ 4 ] claimed that “ it seems unlikely that genomic GC content is driven by thermal adaptation ” after reviewing the results of Hurst and Merchant [ 27 ] and Xia et al [ 28 ], but without mentioning the debate on Musto et al [ 30 ].…”

Section: Introductionmentioning

confidence: 99%

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A positive correlation between GC content and growth temperature in prokaryotes

Lan

Liu

et al. 2022

BMC Genomics

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Background GC pairs are generally more stable than AT pairs; GC-rich genomes were proposed to be more adapted to high temperatures than AT-rich genomes. Previous studies consistently showed positive correlations between growth temperature and the GC contents of structural RNA genes. However, for the whole genome sequences and the silent sites of the codons in protein-coding genes, the relationship between GC content and growth temperature is in a long-lasting debate. Results With a dataset much larger than previous studies (681 bacteria and 155 archaea with completely assembled genomes), our phylogenetic comparative analyses showed positive correlations between optimal growth temperature (Topt) and GC content both in bacterial and archaeal structural RNA genes and in bacterial whole genome sequences, chromosomal sequences, plasmid sequences, core genes, and accessory genes. However, in the 155 archaea, we did not observe a significant positive correlation of Topt with whole-genome GC content (GCw) or GC content at four-fold degenerate sites. We randomly drew 155 samples from the 681 bacteria for 1000 rounds. In most cases (> 95%), the positive correlations between Topt and genomic GC contents became statistically nonsignificant (P > 0.05). This result suggested that the small sample sizes might account for the lack of positive correlations between growth temperature and genomic GC content in the 155 archaea and the bacterial samples of previous studies. Comparing the GC content among four categories (psychrophiles/psychrotrophiles, mesophiles, thermophiles, and hyperthermophiles) also revealed a positive correlation between GCw and growth temperature in bacteria. By including the GCw of incompletely assembled genomes, we expanded the sample size of archaea to 303. Positive correlations between GCw and Topt appear especially after excluding the halophilic archaea whose GC contents might be strongly shaped by intense UV radiation. Conclusions This study explains the previous contradictory observations and ends a long debate. Prokaryotes growing in high temperatures have higher GC contents. Thermal adaptation is one possible explanation for the positive association. Meanwhile, we propose that the elevated efficiency of DNA repair in response to heat mutagenesis might have the by-product of increasing GC content like that happens in intracellular symbionts and marine bacterioplankton.

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“…This genomic trait has been widely studied, and its evolution has been proposed to be associated with numerous mutational and selective forces driven by genetic, metabolic, and ecological factors [ 4 – 19 ]. The high temperature might be the most long-debating [ 20 – 22 ]. Because G:C pairs have an additional hydrogen bond than A:T pairs, the GC-rich genomes are expected to be thermally more stable in high-temperature environments [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A positive correlation between GC content and growth temperature in prokaryotes

Lan

Liu

et al. 2022

BMC Genomics

View full text Add to dashboard Cite

show abstract

“…This genomic trait has been widely studied, and its evolution has been proposed to be associated with numerous mutational and selective forces driven by genetic, metabolic, and ecological factors (Foerstner et al 2005; Hildebrand et al 2010; Mann and Chen 2010; Raghavan et al 2012; Wu et al 2012; Agashe and Shankar 2014; Glemin et al 2014; Šmarda et al 2014; Reichenberger et al 2015; Aslam et al 2019; Dietel et al 2019; Weissman et al 2019; Kogay et al 2020). Among them, the high temperature might be the most long-debating one (Galtier and Lobry 1997; Forsdyke 2021; Meyer 2021). Because G:C pairs have an additional hydrogen bond than A:T pairs, the GC-rich genomes are thermally more stable in high-temperature environments.…”

Section: Introductionmentioning

confidence: 99%

“…Still, this study did not shake the confidence of Musto et al (35) on the correlation between Topt and genomic GC content in prokaryotes. Although Musto and coauthors have rebutted all the criticisms, their studies have not convinced later authors of review articles (4, 20, 36). For example, Agashe and Shankar (4) claimed that “ it seems unlikely that genomic GC content is driven by thermal adaptation ” after reviewing the results of Hurst and Merchant (27) and Xia et al (28), but without mentioning the debates on Musto et al (30).…”

Section: Introductionmentioning

confidence: 99%

“…This genomic trait has been widely studied, and its evolution has been proposed to be associated with numerous mutational and selective forces driven by genetic, metabolic, and ecological factors (4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19). The high temperature might be the most long-debating (20)(21)(22). Because G:C pairs have an additional hydrogen bond than A:T pairs, the GC-rich genomes are expected to be thermally more stable in high-temperature environments (23).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A positive correlation between GC content and growth temperature in prokaryotes

Lan

Liu

et al. 2021

Preprint

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Because GC pairs are more stable than AT pairs, GC-rich sequences were proposed to be more adapted to high temperatures than AT-rich sequences. Previous studies consistently showed positive correlations between the growth temperature and the GC contents of structural RNA genes. However, for the whole genome sequences and the silent sites of the codons in protein-coding genes, the relationship between GC content and growth temperature is in a long-lasting debate. With a dataset much larger than previous studies (681 bacteria and 155 archaea), our phylogenetic comparative analyses showed positive correlations between optimal growth temperature and GC content exists, both in the structural RNA genes of bacteria and archaea and in bacterial whole genome sequences, chromosomal sequences, plasmid sequences, core genes, and accessory genes. However, in the 155 archaea, we did not observe a significant positive correlation of optimal growth temperature with whole-genome GC content or GC content at four-fold degenerate sites. We randomly drew 155 samples from the 681 bacteria for 1000 rounds. In most cases (> 95%), the positive correlations between optimal growth temperature and genomic GC content became statistically nonsignificant (P > 0.05). This result suggested that the small sample sizes might account for the lack of positive correlations between growth temperature and genomic GC content in the 155 archaea and the bacterial samples of previous studies.

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