A comparison between aerobic growth of Bacillus licheniformis in continuous culture and partial-recycling fermentor, with contributions to the discussion on maintenance energy demand

Bulthuis, Ben A.; Koningstein, Gregory M.; Stouthamer, A. H.; Verseveld, Henk W. van

doi:10.1007/bf00446937

Cited by 50 publications

(34 citation statements)

References 33 publications

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“…Higher maintenance requirements exhibited by B. thuringiensis in these complex substrates might be due to one or more maintenance functions, which include cell wall modifications (Hazel and Williams, 1990;Sachidanandham et al, 2005), osmotic balancing of intracellular cation concentrations (Weisser and Truper, 1985), accumulation of elevated levels of intracellular ions such as sodium, potassium, magnesium, calcium, manganese, or chloride in response to their presence in the external media (De-Medicis et al, 1986;Imhoff, 1984;Kamekura and Kushner, 1984;Kushner et al, 1983;Vreeland et al, 1983), modification in the protein synthesis machinery (Choquet et al, 1989;Kamekura and Kushner, 1984;Wydro et al, 1977), changes in the properties of ribosomes (Kogut and Madira, 1978), and reduced carbohydrate transport (Roth et al, 1985a,b) at times demands the use of alternate methods for their studies in bioreactor (Christiansen et al, 2003;Sachidanandham and Gin, 2003). The inverse relationship observed between the values of maintenance coefficient and growth rate among B. thuringiensis and K90, are consistent with observations on several bacterial systems (Arbige and Chesbro, 1982;Bulthuis et al, 1989;Stouthamer et al, 1990;Tappe et al, 1999;van-Verseveld et al, 1984van-Verseveld et al, , 1986. However, the maintenance coefficient of K90, the cryptic Bacillus exhibiting high sequence similarity with B. mojavensis, was found to be significantly lower than Maintenance coefficient, h-1 Specific growth rate, h-1…”

Section: Discussionsupporting

confidence: 83%

A crypticBacillusisolate exhibited narrow 16S rRNA gene sequence divergence withBacillus thuringiensisand showed low maintenance requirements in hyper‐osmotic complex substrate cultivations

Sachidanandham

Al-Shayji

Al-Awadhi

et al. 2005

Biotech & Bioengineering

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A cryptic Bacillus (K90) isolate obtained from soil samples from the Kuwait desert exhibited lower maintenance requirements in complex substrate cultivations than Bacillus thuringiensis. A mathematical model was used to estimate apparent maintenance coefficients (m(c)) and these were found to be 0.336 and 0.041/h for B. thuringiensis and K90, respectively. The results also showed that the values of apparent maintenance coefficients were inversely related to the specific growth rates. Furthermore, 16S rRNA gene sequencing showed that K90 exhibited 99.81% sequence similarity to that of B. mojavensis and 92.9% with B. thuringiensis. It is evident from the dendrogram that the evolution of B. mojavensis (K90) (B. subtilis group), which may have originated after B. licheniformis could have been influenced by prolonged hyper-osmotic conditions, while B. thuringiensis that evolved before B. oleronius exhibited greater sensitivity as implied by the higher maintenance coefficient obtained for the hyper-osmotic cultures. As K90 exhibited low maintenance requirements in hyperosmotic cultures, close phylogenetic relationship with B. thuringiensis, along with the reported property of encapsulation of insecticidal crystal proteins (Cry) in Bacillus strains and endophytic nature of B. mojavensis, strongly suggest that K90 could be a promising surrogate host for the transgenic delivery of "Cry" proteins.

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Section: Discussionsupporting

confidence: 83%

A crypticBacillusisolate exhibited narrow 16S rRNA gene sequence divergence withBacillus thuringiensisand showed low maintenance requirements in hyper‐osmotic complex substrate cultivations

Sachidanandham

Al-Shayji

Al-Awadhi

et al. 2005

Biotech & Bioengineering

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“…This reduced anabolic demand is reflected in the transcriptome of most organisms by a decreased expression of genes involved in biosynthetic routes. Protein synthesis is the most energy-demanding biosynthetic process (26). Under the severe calorie restriction in retentostat cultures, B. subtilis, S. cerevisiae, and A. niger showed reduced expression of components of the translation machinery, including ribosomal proteins and amino acyl tRNA synthases (Fig.…”

Section: Similar Transcriptional Responses In Pathways Involved In Numentioning

confidence: 99%

“…Slow growth of microbes under defined, constant conditions can be studied in chemostat cultures at low dilution rates (23)(24)(25). However, chemostat cultures cannot be used to assess extremely low specific growth rates (Ͻ0.01 h Ϫ1 ), due to technical limitations related to discontinuous substrate addition, the time required for reaching steady state, and the emergence and selection of adapted mutant variants (26,27).…”

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confidence: 99%

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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“…Under these conditions, the cells' metabolism is switched towards the 'NADH-type' respiration which is more energetically effective (more coupled) (Lawford et al, 1976;Artzatbanov et al, 1983). This could provide energy for the increased costs of protein synthesis (Bulthuis et al, 1989) and for the energy-linked transport of substrates whose exogenous concentrations are low. The adaptation of the facultative methylotroph Pseudomoms AM1 to carbon-limited growth induced the synthesis of the membrane-bound cytochrome c, leading to the appearance of an additional coupling site (Keevil & Anthony, 1979).…”

Section: Discussionmentioning

confidence: 99%

The increase of KCN-sensitive electron flow in the branched respiratory chain of Micrococcus luteus grown slowly in carbon-limited culture

Artzatbanov

Sheiko

Lukoyanova

et al. 1991

Journal of General Microbiology

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The strictly aerobic bacterium Micrococcus luteus was grown in the presence of lactate as sole carbon source under conditions of excess substrates (in batch culture) or under strict lactate (C) or ammonium (N) limitation (in a chemostat, D=O.O2 h-l). KCN (2mM) stimulated the respiration of batch-grown and N-limited cells, and inhibited the oxidase activity of C-limited cells by 4040%. The content and composition of dytochromes and the KCN-dependences of the oxidase activities were found to be the same for the membranes of C-limited and batchgrown cells. The KCN sensitivity of the oxidase activities of isolated membranes decreased in the order NADH > malate > lactate. NAD-dependent lactate and malate dehydrogenase activities were observed in the cytoplasm of C-limited cells but not in that of batch-grown cells. The stimulation of cell respiration by lactate, malate, pyruvate or ethanol caused a marked increase of the steady-state level of NAD+ reduction only in Climited cells. It is assumed that the slow growth of C-limited cells is accompanied by an increase in the formation of NADH, which is oxidized by the KCN-sensitive, tightly-coupled, main branch of the M. luteus respiratory chain. Under non-limited conditions of growth the respiration is due mainly to the direct oxidation of lactate via the weakly coupled alternative branch. The role of this switching of the electron flow from one pathway to the other during the adaptation of the bateria to the slow C-and energy-limited growth is discussed.

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A comparison between aerobic growth of Bacillus licheniformis in continuous culture and partial-recycling fermentor, with contributions to the discussion on maintenance energy demand

Cited by 50 publications

References 33 publications

A crypticBacillusisolate exhibited narrow 16S rRNA gene sequence divergence withBacillus thuringiensisand showed low maintenance requirements in hyper‐osmotic complex substrate cultivations

A crypticBacillusisolate exhibited narrow 16S rRNA gene sequence divergence withBacillus thuringiensisand showed low maintenance requirements in hyper‐osmotic complex substrate cultivations

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

The increase of KCN-sensitive electron flow in the branched respiratory chain of Micrococcus luteus grown slowly in carbon-limited culture

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