An optimal growth law for RNA composition and its partial implementation through ribosomal and tRNA gene locations in bacterial genomes

Hu, Xiao-Pan; Lercher, Martin J.

doi:10.1101/2021.02.05.429890

Cited by 2 publications

(5 citation statements)

References 62 publications

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“…On the pathway level, however, proteome allocation to at least one cellular process -protein translation -is optimized for maximal efficiency at the given protein synthesis rate (18)(19)(20)(21). This indicates that while the global allocation of proteins is not always optimized for maximal growth rate, the proteome allocation to some cellular pathways is at a local optimum -i.e., the individual pathway utilizes the minimal protein mass required to support the observed pathway output.…”

Section: Importancementioning

confidence: 99%

Proteome efficiency of metabolic pathways inEscherichia coliincreases along the nutrient flow

Schröder

Lercher

2022

Preprint

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Understanding the allocation of the cellular proteome to different cellular processes is central to unraveling the organizing principles of bacterial physiology. Proteome allocation to protein translation itself is maximally efficient, i.e., it represents the minimal allocation of dry mass able to sustain the observed protein production rate. In contrast, recent studies on bacteria have demonstrated that the concentrations of many proteins exceed the minimal level required to support the observed growth rate, indicating some heterogeneity across pathways in their proteome efficiency. Here, we systematically analyze the proteome efficiency of metabolic pathways, which together account for more than half of the E. coli proteome during exponential growth. Comparing the predicted minimal and the observed proteome allocation to different metabolic pathways across growth conditions, we find that the most costly biosynthesis pathways – those for amino acid biosynthesis and cofactor biosynthesis – are expressed for near optimal efficiency. Overall, proteome efficiency increases along the carbon flow through the metabolic network: proteins involved in pathways of nutrient uptake and central metabolism tend to be highly over-abundant, while proteins involved in anabolic pathways and in protein translation are much closer to the expected minimal abundance across conditions. Our work thus provides a bird's-eye view of metabolic pathway efficiency, demonstrating systematic deviations from optimal cellular efficiency at the network level.

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Section: Importancementioning

confidence: 99%

Proteome efficiency of metabolic pathways inEscherichia coliincreases along the nutrient flow

Schröder

Lercher

2022

Preprint

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“…Increasing evidence suggests that gene order within the bacterial chromosome contributes to cellular homeostasis by coordinating key entangled processes such as chromosome structuration, cell cycle, replication and the expression of genetic information. While genome reshuffling experiments have not been yet performed in bacterial systems (79) approaches such as comparative genomics (17,18,21,23,31,80), systems biology (20), large DNA inversions (81)(82)(83) and relocation of individual gene sets (16,19,(84)(85)(86) have provided support to this notion. Genes encoding for the genetic information flow are interesting models to test the role of genomic position on cellular physiology.…”

Section: Discussionmentioning

confidence: 99%

“…Genes encoding for the genetic information flow are interesting models to test the role of genomic position on cellular physiology. The chromosomal position of rRNA, some tRNAs, RP and RNA polymerase genes is biased towards the oriC , particularly in fast-growing bacteria (17, 22, 24, 51). Relocation of S10, the main RP locus harboring half of its encoding genes, far from oriC constrains bacterial growth (49).…”

Section: Discussionmentioning

confidence: 99%

“…The present work incorporates the evolutionary aspect to studies on positional genetics expanding our knowledge on the long-term implication of gene order on genome evolution. The role of the genomic position of other key genes remain to be explored such as ribosomal RNAs(101), tRNA UBI (22, 24), RNA polymerase(51), ATP synthase(17), among others. This is central to understand how genome’s primary structure impacts cell physiology, in particular growth rate and genome evolution.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies suggest that gene order contributes to link genome structure to cell physiology (14,(16)(17)(18)(19)(20). The genomic position of key gene groups is widely conserved along the oriter axis following the temporal pattern of gene expression (17,18,21,22). Thus, coding sequences expressed in exponential phase are physically associated to the oriC region while factors transcribed in stress situations or in stationary phase cluster close to the ter region (17,21,(23)(24)(25)(26).…”

Section: Introductionmentioning

confidence: 99%

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Chromosomal position of ribosomal protein genes impacts long term evolution ofVibrio cholerae

Mornico

Bernal-Bayard

Ghigo

et al. 2022

Preprint

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It is unclear how gene order within the chromosome influences bacterial evolution. The genomic location of genes encoding the flow of genetic information is biased towards the replication origin (oriC) in fast-growing bacteria. To study the role of chromosomal location on cell physiology we relocated the S10-spec-α locus (S10), harboring half of ribosomal protein genes, to different chromosomal positions in the fast-growing pathogen V. cholerae. We found that growth rate, fitness and infectivity inversely correlated the distance between S10 and oriC. To gain insight into the evolutionary effect of RP genomic position, we evolved strains bearing S10 at its current oriC-proximal location or derivatives harboring the locus far from it (i.e. 1.5Mbp). Populations deep sequencing on average 1 mutation fixed each 100 generations, mainly at genes linked to flagellum regulation, lipopolysaccharide synthesis, chemotaxis, biofilm and quorum sensing. Along the experiment, populations showed an increment in biofilm forming capacity. All populations increased their growth rate. However, growth rate advantage of populations bearing S10 at an oriC-proximal persisted along the experiment over those where the main ribosomal protein gene cluster locates at an oriC-distal position. This indicates that suppressor mutations cannot compensate S10 genomic location. We selected fast-growing clones displaying a ∼10% growth rate increment finding that they harbored inactivating mutations at, among other sites, flagellum master regulators flrAB regardless S10 genomic location. The introduction of these mutations on naïve V. cholerae strains resulted in a ∼10% increase in growth rate. Our study therefore demonstrates that the location of ribosomal protein genes conditions the evolutionary trajectory of growth rate in the long term. While genomic content is highly plastic in prokaryotes, gene order is an underestimated factor that conditions cellular physiology and lineage evolution. The lack of suppression enables artificial gene relocation for genetic circuit reprogramming.

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An optimal growth law for RNA composition and its partial implementation through ribosomal and tRNA gene locations in bacterial genomes

Cited by 2 publications

References 62 publications

Proteome efficiency of metabolic pathways inEscherichia coliincreases along the nutrient flow

Proteome efficiency of metabolic pathways inEscherichia coliincreases along the nutrient flow

Chromosomal position of ribosomal protein genes impacts long term evolution ofVibrio cholerae

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