Very slow growth of Bacillus polymyxa: Stringent response and maintenance energy

Arbige, Michael V.; Chesbro, William

doi:10.1007/bf00413386

Cited by 53 publications

(27 citation statements)

References 17 publications

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“…Contrary to earlier retentostat studies employing other bacteria (28,30,31,33), these experiments did not reveal a stringent response, i.e., the m s values calculated from (near-)zero growth retentostats were in good agreement with those estimated by extrapolation from chemostat cultivations at high dilution rates (5,6,29). For all four microbes, the fraction of the carbon and energy source used for maintenance-associated processes increased from 13 to 31% at the initial of 0.025 h Ϫ1 to above 98% after prolonged retentostat cultivation (Table 2).…”

Section: Energy Metabolism At (Near-)zero Growth Rates: Impact Of Maimentioning

confidence: 61%

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

Ercan

Bisschops

Overkamp

et al. 2015

Appl Environ Microbiol

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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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Section: Energy Metabolism At (Near-)zero Growth Rates: Impact Of Maimentioning

confidence: 61%

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

Ercan

Bisschops

Overkamp

et al. 2015

Appl Environ Microbiol

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“…Biomass accumulation and specific rates of glucose consumption at near-zero growth rates in the retentostat cultures could be accurately predicted based on a maintenance coefficient calculated from chemostat cultures grown at higher specific growth rates (0.025 to 0.20 h Ϫ1 ). This indicates that, in contrast to several prokaryotes that exhibit a stringent response (2,3,49), S. cerevisiae does exhibit a reduced maintenance energy requirement at very low specific growth rates. Further indications that glucose metabolism in S. cerevisiae has not specifically evolved for slow growth under sugar limitation were obtained from the kinetics of glucose consumption in the retentostat cultures.…”

Section: Discussionmentioning

confidence: 99%

Quantitative Physiology of Saccharomyces cerevisiae at Near-Zero Specific Growth Rates

Boender

Hulster

Maris

et al. 2009

Appl Environ Microbiol

103

146

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Growth at near-zero specific growth rates is a largely unexplored area of yeast physiology. To investigate the physiology of Saccharomyces cerevisiae under these conditions, the effluent removal pipe of anaerobic, glucoselimited chemostat culture (dilution rate, 0.025 h ؊1 ) was fitted with a 0.22-m-pore-size polypropylene filter unit. This setup enabled prolonged cultivation with complete cell retention. After 22 days of cultivation, specific growth rates had decreased below 0.001 h ؊1 (doubling time of >700 h). Over this period, viability of the retentostat cultures decreased to ca. 80%. The viable biomass concentration in the retentostats could be accurately predicted by a maintenance coefficient of 0.50 mmol of glucose g ؊1 of biomass h ؊1 calculated from anaerobic, glucose-limited chemostat cultures grown at dilution rates of 0.025 to 0.20 h ؊1 . This indicated that, in contrast to the situation in several prokaryotes, maintenance energy requirements in S. cerevisiae do not substantially change at near-zero specific growth rates. After 22 days of retentostat cultivation, glucose metabolism was predominantly geared toward alcoholic fermentation to meet maintenance energy requirements. The strict correlation between glycerol production and biomass formation observed at higher specific growth rates was not maintained at the near-zero growth rates reached in the retentostat cultures. In addition to glycerol, the organic acids acetate, D-lactate, and succinate were produced at low rates during prolonged retentostat cultivation. This study identifies robustness and by-product formation as key issues in attempts to uncouple growth and product formation in S. cerevisiae.Laboratory studies on microorganisms are often performed in batch cultures. During the initial phase of batch cultivation, all nutrients are usually present in excess. As a consequence, the initial specific growth rate, , of the microorganism in such cultures equals the maximum specific growth rate, max . In natural environments, the specific growth rate of microorganisms is likely to be constrained by the limited availability of one or more growth-limiting nutrients, resulting in specific growth rates far below max (8,24). In chemostat cultures fed with a medium containing a single growth-limiting nutrient, the dilution rate determines the specific growth rate. Chemostat cultivation therefore offers the possibility to study microbial physiology at carefully controlled, submaximal specific growth rates and to investigate the effect of specific growth rate on cellular physiology (20). Chemostat cultivation of the yeast Saccharomyces cerevisiae has demonstrated strong effects of specific growth rate on biomass composition (26, 51), product formation (5, 37), and cell size (23). Moreover, during energy-limited growth at low specific growth rates, a relatively large fraction of the energy substrate has to be dissimilated for maintenancerelated processes such as maintenance of chemi-osmotic gradients and turnover of cellular components (34). Not surprisi...

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“…Moreover, under stressful conditions, bacteria might adjust their metabolic processes and decelerate their requirements for maintenance energy. This phenomenon is observed as a decrease in the specific activity (Arbrige and Chesbro, 1982). Takdastan et al (2009) also found low SOUR values (average of 3 mg O 2 /g VSS·h) at chlorine dosages of 20 mg/g MLSS.…”

Section: Respirometry Microscopy and Toxicity Resultsmentioning

confidence: 93%

Reduction of Excess Sludge Production in an Activated Sludge System Based on Lysis-Cryptic Growth, Uncoupling Metabolism and Folic Acid Addition

Velho

Daudt

Martins

et al. 2016

Braz. J. Chem. Eng.

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-The following sludge reduction alternatives were tested in wastewater biological reactors: oxic-settling-anaerobic (OSA-process); ultrasonic disintegration (UD); chlorination (CH); 3,3',4',5-tetrachlorosalicylanilide (TCS); and folic acid (FA). Compared to the control system, UD reduced 55% of the sludge production, and greater substrate and nutrient removal efficiency was achieved. CH worsened the sludge settleability and increased the SVI values; the system achieved 25% of sludge reduction. OSA showed 50% and 60% of sludge reduction after 16 and 10 hours under anaerobic conditions, respectively. The observed sludge yield during TCS addition was decreased by 40%, and the sludge settleability worsened. FA presented the highest sludge reduction (75%), and the system improved the nutrient removal efficiency by 30% compared to the control system and maintained the sludge properties. Acute toxicity conducted with Daphnia magna classified the effluent from the sludge reduction systems as non-toxic for discharge into water sources.

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Very slow growth of Bacillus polymyxa: Stringent response and maintenance energy

Cited by 53 publications

References 17 publications

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

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

Quantitative Physiology of Saccharomyces cerevisiae at Near-Zero Specific Growth Rates

Reduction of Excess Sludge Production in an Activated Sludge System Based on Lysis-Cryptic Growth, Uncoupling Metabolism and Folic Acid Addition

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