Physiology, fast and slow: bacterial response to variable resource stoichiometry and dilution rate
Open Access
- 20 August 2024
- journal article
- research article
- Published by American Society for Microbiology in mSystems
- Vol. 9 (8) , e0077024
Abstract
Microorganisms grow despite imbalances in the availability of nutrients and energy. The biochemical and elemental adjustments that bacteria employ to sustain growth when these resources are suboptimal are not well understood. We assessed how Pseudomonas putida KT2440 adjusts its physiology at differing dilution rates (to approximate growth rates) in response to carbon (C), nitrogen (N), and phosphorus (P) stress using chemostats. Cellular elemental and biomolecular pools were variable in response to different limiting resources at a slow dilution rate of 0.12 h −1 , but these pools were more similar across treatments at a faster rate of 0.48 h −1 . At slow dilution rates, limitation by P and C appeared to alter cell growth efficiencies as reflected by changes in cellular C quotas and rates of oxygen consumption, both of which were highest under P- and lowest under C- stress. Underlying these phenotypic changes was differential gene expression of terminal oxidases used for ATP generation that allows for increased energy generation efficiency. In all treatments under fast dilution rates, KT2440 formed aggregates and biofilms, a physiological response that hindered an accurate assessment of growth rate, but which could serve as a mechanism that allows cells to remain in conditions where growth is favorable. Our findings highlight the ways that microorganisms dynamically adjust their physiology under different resource supply conditions, with distinct mechanisms depending on the limiting resource at slow growth and convergence toward an aggregative phenotype with similar compositions under conditions that attempt to force fast growth. IMPORTANCE: All organisms experience suboptimal growth conditions due to low nutrient and energy availability. Their ability to survive and reproduce under such conditions determines their evolutionary fitness. By imposing suboptimal resource ratios under different dilution rates on the model organism Pseudomonas putida KT2440, we show that this bacterium dynamically adjusts its elemental composition, morphology, pools of biomolecules, and levels of gene expression. By examining the ability of bacteria to respond to C:N:P imbalance, we can begin to understand how stoichiometric flexibility manifests at the cellular level and impacts the flow of energy and elements through ecosystems.Keywords
Funding Information
- National Science Foundation (DEB-1930816)
This publication has 145 references indexed in Scilit:
- Adenosine triphosphate (ATP) as a metric of microbial biomass in aquatic systems: new simplified protocols, laboratory validation, and a reflection on data from the literatureLimnology and Oceanography: Methods, 2021
- Engineering Native and Synthetic Pathways in Pseudomonas putida for the Production of Tailored PolyhydroxyalkanoatesBiotechnology Journal, 2020
- Growth rate and resource imbalance interactively control biomass stoichiometry and elemental quotas of aquatic bacteriaEcology, 2017
- Colony morphology and transcriptome profiling of Pseudomonas putida KT2440 and its mutants deficient in alginate or all EPS synthesis under controlled matric potentialsMicrobiologyopen, 2014
- The Pseudomonas putida Crc global regulator controls the hierarchical assimilation of amino acids in a complete medium: Evidence from proteomic and genomic analysesProteomics, 2009
- Production of medium-chain-length polyhydroxyalkanoates by high-cell-density cultivation ofPseudomonas putida under phosphorus limitationBiotechnology and Bioengineering, 2000
- Ribosome Modulation Factor: Stationary Growth Phase-Specific Inhibitor of Ribosome Functions from Escherichia coliBiochemical and Biophysical Research Communications, 1995
- Gene regulation by phosphate in enteric bacteriaJournal of Cellular Biochemistry, 1993
- Estimation of the biofilm formation ability of Pseudomonas putida in discrete samples from continuous cultureApplied Microbiology and Biotechnology, 1984
- The impact of dilution rate and attached growth on steady-state characteristics of Pseudomonas putidaApplied Microbiology and Biotechnology, 1981