Deciphering the Principles of Bacterial Nitrogen Dietary Preferences: a Strategy for Nutrient Containment.

Jilong Wang,Yi-Ping Wang,Ray Dixon,Dalai Yan,Caroline S Harwood

doi:10.1128/mbio.00792-16

Jilong Wang, Yi-Ping Wang + Show 3 more

Open Access

https://doi.org/10.1128/mbio.00792-16

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Journal: mBio	Publication Date: Jul 19, 2016
Citations: 28	License type: CC BY 4.0

Affiliation: Peking University, John Innes Centre, Indiana University

Abstract

ABSTRACTA fundamental question in microbial physiology concerns why organisms prefer certain nutrients to others. For example, among different nitrogen sources, ammonium is the preferred nitrogen source, supporting fast growth, whereas alternative nitrogen sources, such as certain amino acids, are considered to be poor nitrogen sources, supporting much slower exponential growth. However, the physiological/regulatory logic behind such nitrogen dietary choices remains elusive. In this study, by engineering Escherichia coli, we switched the dietary preferences toward amino acids, with growth rates equivalent to that of the wild-type strain grown on ammonia. However, when the engineered strain was cultured together with wild-type E. coli, this growth advantage was diminished as a consequence of ammonium leakage from the transport-and-catabolism (TC)-enhanced (TCE) cells, which are preferentially utilized by wild-type bacteria. Our results reveal that the nitrogen regulatory (Ntr) system fine tunes the expression of amino acid transport and catabolism components to match the flux through the ammonia assimilation pathway such that essential nutrients are retained, but, as a consequence, the fast growth rate on amino acids is sacrificed.

Highlights

A fundamental question in microbial physiology concerns why organisms prefer certain nutrients to others
We report a direct correlation between nitrogen influx (JN) and growth rate in E. coli, regardless of the nitrogen source used, and demonstrate that the slow growth rate on specific amino acids is limited by constraints on transport and catabolism, as anticipated [17]
On the basis of the linear growth rate relationship shown in Fig. 1A, we propose that the phenotype of slow growth on alternative nitrogen sources relates to the level of JN, as depicted in the metabolism-regulation model (Fig. 1B)

Summary

Introduction

A fundamental question in microbial physiology concerns why organisms prefer certain nutrients to others. We demonstrated that in the absence of regulatory feedback, amino acids are capable of supporting fast growth rates, but this results in ammonia leaking out from cells as “waste,” benefiting the growth of competitors. These findings provide important insights into the regulatory logic that controls metabolic flux and ensures nutrient containment but sacrifices growth rate. Under nitrogen-limiting conditions, GlnD covalently modifies GlnB, enabling NtrB to phosphorylate NtrC, which activates Ntr-dependent genes, including the expression of glnK (which encodes GlnK). It has been confirmed that the Ntr system maintains a fast growth rate across a wide range of ammonium concentrations, primarily by regulating both the expression and activity of the glutamine synthesis enzyme GS (glutamine synthetase) and of the ammonium transporter AmtB [5, 14,15,16]

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