Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
Abstract Background In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. R...
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| Format: | Article |
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BMC
2020-04-01
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| Series: | BMC Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12915-020-00777-5 |
| _version_ | 1818153848242438144 |
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| author | Alfonso Soler-Bistué Sebastián Aguilar-Pierlé Marc Garcia-Garcerá Marie-Eve Val Odile Sismeiro Hugo Varet Rodrigo Sieira Evelyne Krin Ole Skovgaard Diego J. Comerci Eduardo P. C. Rocha Didier Mazel |
| author_facet | Alfonso Soler-Bistué Sebastián Aguilar-Pierlé Marc Garcia-Garcerá Marie-Eve Val Odile Sismeiro Hugo Varet Rodrigo Sieira Evelyne Krin Ole Skovgaard Diego J. Comerci Eduardo P. C. Rocha Didier Mazel |
| author_sort | Alfonso Soler-Bistué |
| collection | DOAJ |
| description | Abstract Background In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. Relocation of s10-spc-α locus (S10), which codes for most of the RP, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction on its dosage, its expression, and bacterial growth rate. However, a mechanism linking S10 dosage to cell physiology has still not been determined. Results We hypothesized that S10 dosage perturbations impact protein synthesis capacity. Strikingly, we observed that in Vibrio cholerae, protein production capacity was independent of S10 position. Deep sequencing revealed that S10 relocation altered chromosomal replication dynamics and genome-wide transcription. Such changes increased as a function of oriC-S10 distance. Since RP constitutes a large proportion of cell mass, lower S10 dosage could lead to changes in macromolecular crowding, impacting cell physiology. Accordingly, cytoplasm fluidity was higher in mutants where S10 is most distant from oriC. In hyperosmotic conditions, when crowding differences are minimized, the growth rate and replication dynamics were highly alleviated in these strains. Conclusions The genomic location of RP genes ensures its optimal dosage. However, besides of its essential function in translation, their genomic position sustains an optimal macromolecular crowding essential for maximizing growth. Hence, this could be another mechanism coordinating DNA replication to bacterial growth. |
| first_indexed | 2024-12-11T14:17:08Z |
| format | Article |
| id | doaj.art-0e46f0997c7e457d9ba2526935b7d3fc |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-11T14:17:08Z |
| publishDate | 2020-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-0e46f0997c7e457d9ba2526935b7d3fc2022-12-22T01:03:06ZengBMCBMC Biology1741-70072020-04-0118111810.1186/s12915-020-00777-5Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio choleraeAlfonso Soler-Bistué0Sebastián Aguilar-Pierlé1Marc Garcia-Garcerá2Marie-Eve Val3Odile Sismeiro4Hugo Varet5Rodrigo Sieira6Evelyne Krin7Ole Skovgaard8Diego J. Comerci9Eduardo P. C. Rocha10Didier Mazel11Institut Pasteur, Unité Plasticité du Génome Bactérien, UMR3525, CNRSInstitut Pasteur, Unité Plasticité du Génome Bactérien, UMR3525, CNRSMicrobial Evolutionary Genomics, Département Génomes et Génétique, Institut PasteurInstitut Pasteur, Unité Plasticité du Génome Bactérien, UMR3525, CNRSInstitut Pasteur, Plate-forme Transcriptome et Épigenome, Biomics, Centre d’Innovation et Recherche Technologique (Citech)Institut Pasteur, Plate-forme Transcriptome et Épigenome, Biomics, Centre d’Innovation et Recherche Technologique (Citech)Fundación Instituto Leloir, IIBBA-CONICETInstitut Pasteur, Unité Plasticité du Génome Bactérien, UMR3525, CNRSDepartment of Science and Environment, Roskilde UniversityInstituto de Investigaciones Biotecnológicas “Dr. Rodolfo A. Ugalde,” CONICET - Universidad Nacional de San MartínMicrobial Evolutionary Genomics, Département Génomes et Génétique, Institut PasteurInstitut Pasteur, Unité Plasticité du Génome Bactérien, UMR3525, CNRSAbstract Background In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. Relocation of s10-spc-α locus (S10), which codes for most of the RP, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction on its dosage, its expression, and bacterial growth rate. However, a mechanism linking S10 dosage to cell physiology has still not been determined. Results We hypothesized that S10 dosage perturbations impact protein synthesis capacity. Strikingly, we observed that in Vibrio cholerae, protein production capacity was independent of S10 position. Deep sequencing revealed that S10 relocation altered chromosomal replication dynamics and genome-wide transcription. Such changes increased as a function of oriC-S10 distance. Since RP constitutes a large proportion of cell mass, lower S10 dosage could lead to changes in macromolecular crowding, impacting cell physiology. Accordingly, cytoplasm fluidity was higher in mutants where S10 is most distant from oriC. In hyperosmotic conditions, when crowding differences are minimized, the growth rate and replication dynamics were highly alleviated in these strains. Conclusions The genomic location of RP genes ensures its optimal dosage. However, besides of its essential function in translation, their genomic position sustains an optimal macromolecular crowding essential for maximizing growth. Hence, this could be another mechanism coordinating DNA replication to bacterial growth.http://link.springer.com/article/10.1186/s12915-020-00777-5Ribosomal proteinsMacromolecular crowdingGrowth rateVibrio choleraeBacterial chromosomeBacterial physiology |
| spellingShingle | Alfonso Soler-Bistué Sebastián Aguilar-Pierlé Marc Garcia-Garcerá Marie-Eve Val Odile Sismeiro Hugo Varet Rodrigo Sieira Evelyne Krin Ole Skovgaard Diego J. Comerci Eduardo P. C. Rocha Didier Mazel Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae BMC Biology Ribosomal proteins Macromolecular crowding Growth rate Vibrio cholerae Bacterial chromosome Bacterial physiology |
| title | Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae |
| title_full | Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae |
| title_fullStr | Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae |
| title_full_unstemmed | Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae |
| title_short | Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae |
| title_sort | macromolecular crowding links ribosomal protein gene dosage to growth rate in vibrio cholerae |
| topic | Ribosomal proteins Macromolecular crowding Growth rate Vibrio cholerae Bacterial chromosome Bacterial physiology |
| url | http://link.springer.com/article/10.1186/s12915-020-00777-5 |
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