A positive correlation between GC content and growth temperature in prokaryotes
Abstract 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...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-02-01
|
| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-022-08353-7 |
| _version_ | 1819277033923936256 |
|---|---|
| author | En-Ze Hu Xin-Ran Lan Zhi-Ling Liu Jie Gao Deng-Ke Niu |
| author_facet | En-Ze Hu Xin-Ran Lan Zhi-Ling Liu Jie Gao Deng-Ke Niu |
| author_sort | En-Ze Hu |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-23T23:49:41Z |
| format | Article |
| id | doaj.art-98fa216b26b641d7a8c71977879883ee |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-23T23:49:41Z |
| publishDate | 2022-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-98fa216b26b641d7a8c71977879883ee2022-12-21T17:25:26ZengBMCBMC Genomics1471-21642022-02-0123111710.1186/s12864-022-08353-7A positive correlation between GC content and growth temperature in prokaryotesEn-Ze Hu0Xin-Ran Lan1Zhi-Ling Liu2Jie Gao3Deng-Ke Niu4MOE Key Laboratory for Biodiversity Science and Ecological Engineering and Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Sciences, Beijing Normal UniversityMOE Key Laboratory for Biodiversity Science and Ecological Engineering and Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Sciences, Beijing Normal UniversityMOE Key Laboratory for Biodiversity Science and Ecological Engineering and Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Sciences, Beijing Normal UniversityMOE Key Laboratory for Biodiversity Science and Ecological Engineering and Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Sciences, Beijing Normal UniversityMOE Key Laboratory for Biodiversity Science and Ecological Engineering and Beijing Key Laboratory of Gene Resource and Molecular Development, College of Life Sciences, Beijing Normal UniversityAbstract 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.https://doi.org/10.1186/s12864-022-08353-7GC contentOptimal growth temperatureProkaryotesEvolutionThermophile |
| spellingShingle | En-Ze Hu Xin-Ran Lan Zhi-Ling Liu Jie Gao Deng-Ke Niu A positive correlation between GC content and growth temperature in prokaryotes BMC Genomics GC content Optimal growth temperature Prokaryotes Evolution Thermophile |
| title | A positive correlation between GC content and growth temperature in prokaryotes |
| title_full | A positive correlation between GC content and growth temperature in prokaryotes |
| title_fullStr | A positive correlation between GC content and growth temperature in prokaryotes |
| title_full_unstemmed | A positive correlation between GC content and growth temperature in prokaryotes |
| title_short | A positive correlation between GC content and growth temperature in prokaryotes |
| title_sort | positive correlation between gc content and growth temperature in prokaryotes |
| topic | GC content Optimal growth temperature Prokaryotes Evolution Thermophile |
| url | https://doi.org/10.1186/s12864-022-08353-7 |
| work_keys_str_mv | AT enzehu apositivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT xinranlan apositivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT zhilingliu apositivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT jiegao apositivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT dengkeniu apositivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT enzehu positivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT xinranlan positivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT zhilingliu positivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT jiegao positivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes AT dengkeniu positivecorrelationbetweengccontentandgrowthtemperatureinprokaryotes |