Molecular Basis of Bacterial Longevity.

Kieran B Pechter,Yasuhiro Oda,Larry Gallagher,Colin Manoil,Jianming Yang,Caroline S Harwood,Liang Yin,Marvin Whiteley

doi:10.1128/mbio.01726-17

Kieran B Pechter, Yasuhiro Oda + Show 6 more

Open Access

https://doi.org/10.1128/mbio.01726-17

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Journal: mBio	Publication Date: Nov 28, 2017
Citations: 24	License type: CC BY 4.0

Affiliation: University of Washington, Qingdao Agricultural University

Abstract

ABSTRACTIt is well known that many bacteria can survive in a growth-arrested state for long periods of time, on the order of months or even years, without forming dormant structures like spores or cysts. How is such longevity possible? What is the molecular basis of such longevity? Here we used the Gram-negative phototrophic alphaproteobacterium Rhodopseudomonas palustris to identify molecular determinants of bacterial longevity. R. palustris maintained viability for over a month after growth arrest due to nutrient depletion when it was provided with light as a source of energy. In transposon sequencing (Tn-seq) experiments, we identified 117 genes that were required for long-term viability of nongrowing R. palustris cells. Genes in this longevity gene set are annotated to play roles in a number of cellular processes, including DNA repair, tRNA modification, and the fidelity of protein synthesis. These genes are critically important only when cells are not growing. Three genes annotated to affect translation or posttranslational modifications were validated as bona fide longevity genes by mutagenesis and complementation experiments. These genes and others in the longevity gene set are broadly conserved in bacteria. This raises the possibility that it will be possible to define a core set of longevity genes common to many bacterial species.

Highlights

It is well known that many bacteria can survive in a growth-arrested state for long periods of time, on the order of months or even years, without forming dormant structures like spores or cysts
We present and validate the phototrophic bacterium Rhodopseudomonas palustris as a model system for identification of genes required for the longevity of nongrowing bacteria
6.4 Ϯ 0.2 7.2 Ϯ 0.9 6.3 Ϯ 0.1 8.1 Ϯ 0.3 mbio.asm.org 7 energy limitation is a common cause of growth arrest for heterotrophic bacteria in natural environments

Summary

Introduction

It is well known that many bacteria can survive in a growth-arrested state for long periods of time, on the order of months or even years, without forming dormant structures like spores or cysts. Nongrowing cultures of Gram-negative bacteria are typically established by supplying a resource such as carbon, nitrogen, or oxygen in a growth-limiting amount [6, 13] Studies of such cultures have informed us about general strategies that bacteria use to persist in a growth-arrested state, including scavenging nutrients, using endogenous storage compounds like glycogen, or degrading cellular components such as lipids to maintain viability [13, 14]. Because of the importance of having an energy supply to maintain viability, many species of bacteria exhibit a large decrease in viability following an initial period of growth arrest This has been well documented for Escherichia coli, for which a small fraction of a growtharrested population will survive after an initial die-off in a cycle of growth and death by feeding on the nutrients released from dead cells [1, 13, 14, 19]. This failure of most cells to survive long-term starvation as a homogenous population may explain why E. coli has not served as a good model for discovery of bacterial longevity genes

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