Physiological and Transcriptional Responses of Different Industrial Microbes at Near-Zero Specific Growth Rates

Abstract

The current knowledge of the physiology and gene expression of industrially relevant microorganisms is largely based on laboratory studies under conditions of rapid growth and high metabolic activity. However, in natural ecosystems and industrial processes, microbes frequently encounter severe calorie restriction. As a consequence, microbial growth rates in such settings can be extremely slow and even approach zero. Furthermore, uncoupling microbial growth from product formation, while cellular integrity and activity are maintained, offers perspectives that are economically highly interesting. Retentostat cultures have been employed to investigate microbial physiology at (near-)zero growth rates. This minireview compares information from recent physiological and gene expression studies on retentostat cultures of the industrially relevant microorganisms Lactobacillus plantarum, Lactococcus lactis, Bacillus subtilis, Saccharomyces cerevisiae, and Aspergillus niger. Shared responses of these organisms to (near-)zero growth rates include increased stress tolerance and a downregulation of genes involved in protein synthesis. Other adaptations, such as changes in morphology and (secondary) metabolite production, were species specific. This comparison underlines the industrial and scientific significance of further research on microbial (near-)zero growth physiology. Most research in microbial physiology focuses on growing cells, although under natural and industrial conditions, microbes frequently encounter a state in which neither growth nor deterioration of cells occurs. However, the experimental design to study microbes in this clearly relevant physiological state is far from trivial.In this minireview, we define zero growth as a nongrowing state in which the viability and metabolic activity of a microbial culture are maintained for prolonged periods. As such, zero growth differs from starvation, which is coupled to cellular deterioration, loss of activity, and ultimately, cell death (1, 2). Zero growth also differs from differentiated survival states, such as bacterial or fungal spores, in which metabolism comes to a standstill (3). Conversely, under zero-growth conditions, microbes exclusively use available substrates for processes that contribute to maintenance of cellular integrity and homeostasis (4-7). Such processes include homeostasis of transmembrane gradients of protons and solutes, defense and repair systems, osmoregulation, and protein turnover (8, 9).In classical food fermentation processes, (near-)zero growth occurs during prolonged periods of extremely restricted availability of energy substrates. Examples include cheese ripening by lactic acid bacteria (LAB) (10-12), wine fermentation by Saccharomyces cerevisiae (13,14), and natto fermentation by Bacillus subtilis (15). Despite the severely energy-limiting conditions, microbes manage to survive in these processes for many weeks, while continuing to produce aroma and flavor compounds in the product matrix (10,13,15,16). Another incentive for studying...

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