The physiology of growth arrest: uniting molecular and environmental microbiology

Abstract

Most bacteria spend the majority of their time in prolonged states of very low metabolic activity and little or no growth, in which electron donors, electron acceptors and/or nutrients are limited, but cells are poised to undergo rapid division cycles when resources become available. These non-growing states are far less studied than other growth states, which leaves many questions regarding basic bacterial physiology unanswered. In this Review, we discuss findings from a small but diverse set of systems that have been used to investigate how growth-arrested bacteria adjust metabolism, regulate transcription and translation, and maintain their chromosomes. We highlight major questions that remain to be addressed, and suggest that progress in answering them will be aided by recent methodological advances and by dialectic between environmental and molecular microbiology perspectives.

Cell morphology drives spatial patterning in microbial communities

“…In natural biofilms, rapid cell growth is often limited to the upper regions of a biofilm (28,41), which will select for coccal morphologies. Indeed, this selective pressure provides a rationale for morphological transitions associated with biofilm development (46)(47)(48) and may partly explain the ubiquity of the coccal morphology despite disadvantages, such as decreased nutrient absorption area (7).…”

Genomewide Dam Methylation in Escherichia coli during Long-Term Stationary Phase

“…LTSP is unique in that populations that survive death phase begin to actively replicate, although at a lower rate than occurs during exponential phase. This period of the bacterial life cycle encompasses many physiological and environmental changes that reflect what E. coli may experience in more natural environments (20–25). Using single-molecule real-time (SMRT) sequencing, we determined whether E. coli prioritizes methylating its genome while in LTSP when cells are under nutrient limitation but subpopulations of cells are beginning to replicate again.…”

“…Using single-molecule real-time (SMRT) sequencing, we determined whether E. coli prioritizes methylating its genome while in LTSP when cells are under nutrient limitation but subpopulations of cells are beginning to replicate again. Subpopulations of cells during LTSP are known to be replicating because of the expression of the growth advantage in stationary phase (GASP) phenotype, where populations that have been aged in batch culture can outcompete parental strains (20, 25). Although cell density measurements remain the same in LTSP, the population is dynamic as selective sweeps, where initial populations are essentially replaced, are occurring under these conditions.…”

Severely Heat Injured Survivors of E. coli O157:H7 ATCC 43888 Display Variable and Heterogeneous Stress Resistance Behavior

“…Indeed, while the heat shock response is well-studied and documented in mildly heat-shocked and therefore more uniformly behaving E. coli populations (Chung et al, 2006), it unfortunately remains cryptic whether and how the dynamics of this response can be extrapolated to the small number of cells within a population that manage to survive a severe heat shock. In fact, this ties in with the more general deficit in our understanding of microbial non-growth states (Bergkessel et al, 2016), and it will be interesting to see how the physiology of cells in the persister or the viable-but-non-culturable state would differ from that of sublethally injured resuscitating cells.…”