Plasticity of growth laws tunes resource allocation strategies in bacteria.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
08 Jan 2024
Historique:
received: 04 08 2023
accepted: 04 12 2023
medline: 8 1 2024
pubmed: 8 1 2024
entrez: 8 1 2024
Statut: aheadofprint

Résumé

Bacteria like E. coli grow at vastly different rates on different substrates, however, the precise reason for this variability is poorly understood. Different growth rates have been attributed to 'nutrient quality', a key parameter in bacterial growth laws. However, it remains unclear to what extent nutrient quality is rooted in fundamental biochemical constraints like the energy content of nutrients, the protein cost required for their uptake and catabolism, or the capacity of the plasma membrane for nutrient transporters. Here, we show that while nutrient quality is indeed reflected in protein investment in substrate-specific transporters and enzymes, this is not a fundamental limitation on growth rate, at least for certain 'poor' substrates. We show that it is possible to turn mannose, one of the 'poorest' substrates of E. coli, into one of the 'best' substrates by reengineering chromosomal promoters of the mannose transporter and metabolic enzymes required for mannose degradation. This result falls in line with previous observations of more subtle growth rate improvement for many other carbon sources. However, we show that this faster growth rate comes at the cost of diverse cellular capabilities, reflected in longer lag phases, worse starvation survival and lower motility. We show that addition of cAMP to the medium can rescue these phenotypes but imposes a corresponding growth cost. Based on these data, we propose that nutrient quality is largely a self-determined, plastic property that can be modulated by the fraction of proteomic resources devoted to a specific substrate in the much larger proteome sector of catabolically activated genes. Rather than a fundamental biochemical limitation, nutrient quality reflects resource allocation decisions that are shaped by evolution in specific ecological niches and can be quickly adapted if necessary.

Identifiants

pubmed: 38190385
doi: 10.1371/journal.pcbi.1011735
pii: PCOMPBIOL-D-23-01241
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011735

Informations de copyright

Copyright: © 2024 Mukherjee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Avik Mukherjee (A)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Yu-Fang Chang (YF)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Yanqing Huang (Y)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Nina Catherine Benites (NC)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Leander Ammar (L)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Jade Ealy (J)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Mark Polk (M)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Markus Basan (M)

Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America.

Classifications MeSH