Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions
The genomic, environmental, and evolutionary interruptions caused the changes in bacterial growth, which were stringently associated with changes in gene expression. The growth and gene expression changes remained unclear in response to these interruptions that occurred combinative. As a pilot study...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-03-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145673/full |
| _version_ | 1797865945509658624 |
|---|---|
| author | Yuichiro Matsui Motoki Nagai Bei-Wen Ying |
| author_facet | Yuichiro Matsui Motoki Nagai Bei-Wen Ying |
| author_sort | Yuichiro Matsui |
| collection | DOAJ |
| description | The genomic, environmental, and evolutionary interruptions caused the changes in bacterial growth, which were stringently associated with changes in gene expression. The growth and gene expression changes remained unclear in response to these interruptions that occurred combinative. As a pilot study, whether and how bacterial growth was affected by the individual and dual interruptions of genome reduction, environmental stress, and adaptive evolution were investigated. Growth assay showed that the presence of the environmental stressors, i.e., threonine and chloramphenicol, significantly decreased the growth rate of the wild-type Escherichia coli, whereas not that of the reduced genome. It indicated a canceling effect in bacterial growth due to the dual interruption of the genomic and environmental changes. Experimental evolution of the reduced genome released the canceling effect by improving growth fitness. Intriguingly, the transcriptome architecture maintained a homeostatic chromosomal periodicity regardless of the genomic, environmental, and evolutionary interruptions. Negative epistasis in transcriptome reorganization was commonly observed in response to the dual interruptions, which might contribute to the canceling effect. It was supported by the changes in the numbers of differentially expressed genes (DEGs) and the enriched regulons and functions. Gene network analysis newly constructed 11 gene modules, one out of which was correlated to the growth rate. Enrichment of DEGs in these modules successfully categorized them into three types, i.e., conserved, responsive, and epistatic. Taken together, homeostasis in transcriptome architecture was essential to being alive, and it might be attributed to the negative epistasis in transcriptome reorganization and the functional differentiation in gene modules. The present study directly connected bacterial growth fitness with transcriptome reorganization and provided a global view of how microorganisms responded to genomic, environmental, and evolutionary interruptions for survival from wild nature. |
| first_indexed | 2024-04-09T23:17:27Z |
| format | Article |
| id | doaj.art-54e1cf990d8049a5b0ce55ebc7d8a5c0 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-09T23:17:27Z |
| publishDate | 2023-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-54e1cf990d8049a5b0ce55ebc7d8a5c02023-03-22T05:40:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-03-011410.3389/fmicb.2023.11456731145673Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptionsYuichiro MatsuiMotoki NagaiBei-Wen YingThe genomic, environmental, and evolutionary interruptions caused the changes in bacterial growth, which were stringently associated with changes in gene expression. The growth and gene expression changes remained unclear in response to these interruptions that occurred combinative. As a pilot study, whether and how bacterial growth was affected by the individual and dual interruptions of genome reduction, environmental stress, and adaptive evolution were investigated. Growth assay showed that the presence of the environmental stressors, i.e., threonine and chloramphenicol, significantly decreased the growth rate of the wild-type Escherichia coli, whereas not that of the reduced genome. It indicated a canceling effect in bacterial growth due to the dual interruption of the genomic and environmental changes. Experimental evolution of the reduced genome released the canceling effect by improving growth fitness. Intriguingly, the transcriptome architecture maintained a homeostatic chromosomal periodicity regardless of the genomic, environmental, and evolutionary interruptions. Negative epistasis in transcriptome reorganization was commonly observed in response to the dual interruptions, which might contribute to the canceling effect. It was supported by the changes in the numbers of differentially expressed genes (DEGs) and the enriched regulons and functions. Gene network analysis newly constructed 11 gene modules, one out of which was correlated to the growth rate. Enrichment of DEGs in these modules successfully categorized them into three types, i.e., conserved, responsive, and epistatic. Taken together, homeostasis in transcriptome architecture was essential to being alive, and it might be attributed to the negative epistasis in transcriptome reorganization and the functional differentiation in gene modules. The present study directly connected bacterial growth fitness with transcriptome reorganization and provided a global view of how microorganisms responded to genomic, environmental, and evolutionary interruptions for survival from wild nature.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145673/fullnegative epistasistranscriptome reorganizationgene networkchromosomal periodicitygenome reductionenvironmental stress |
| spellingShingle | Yuichiro Matsui Motoki Nagai Bei-Wen Ying Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions Frontiers in Microbiology negative epistasis transcriptome reorganization gene network chromosomal periodicity genome reduction environmental stress |
| title | Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions |
| title_full | Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions |
| title_fullStr | Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions |
| title_full_unstemmed | Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions |
| title_short | Growth rate-associated transcriptome reorganization in response to genomic, environmental, and evolutionary interruptions |
| title_sort | growth rate associated transcriptome reorganization in response to genomic environmental and evolutionary interruptions |
| topic | negative epistasis transcriptome reorganization gene network chromosomal periodicity genome reduction environmental stress |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145673/full |
| work_keys_str_mv | AT yuichiromatsui growthrateassociatedtranscriptomereorganizationinresponsetogenomicenvironmentalandevolutionaryinterruptions AT motokinagai growthrateassociatedtranscriptomereorganizationinresponsetogenomicenvironmentalandevolutionaryinterruptions AT beiwenying growthrateassociatedtranscriptomereorganizationinresponsetogenomicenvironmentalandevolutionaryinterruptions |