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Microbial Stress Response as a Tool for Biotechnology

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Microbial Biotechnology".

Deadline for manuscript submissions: closed (30 April 2021) | Viewed by 37008

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Prof. Dr. Ivana Márová

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Guest Editor

Vysoke Uceni Technicke v Brne, Faculty of Chemistry, Brno, Czech Republic
Interests: stress response in bacteria and yeasts; production of stress metabolites in carotenogenic yeasts; production of PHA-based bioplastics under stress; biorefinery concept

Dr. Volha Shapaval

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Guest Editor

Faculty of Science and Technology, Norwegian University of Life Sciences, Droebakveien, Aas, Norway
Interests: green process engineering; bioprocesses and biosystems; process monitoring and optimization of bio-processes; vibrational spectroscopy; monitoring of microorganisms in processing environments
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Dear Colleagues,

Microorganisms are easily grown unicellular ubiquitous organisms, occurring in soil, fresh and marine water, animals, on plants, and in foods. The environment presents for microbes a source of nutrients and forms a space for their growth and metabolism. On the other hand, microbial cells are continuously exposed to a myriad of changes in environmental conditions. These conditions determine the metabolic activity, growth, and survival of cells. Basic knowledge of the effect of environmental factors on microorganisms is important for understanding the ecology and biodiversity of microbes as well as for control the microbial physiology in order to enhance the exploitation of microorganisms or to inhibit or stop their harmful and deleterious activity.

Through thousands of years of evolution, microbes have acquired a number of self-protective mechanisms in order to survive and adapt to a range of environments. To resist environmental stresses, microorganisms maintain the integrity and fluidity of cell membranes by modulating their structure and composition, and the permeability and activities of transporters are adjusted to control nutrient transport and ion exchange. Certain transcription factors are activated to enhance gene expression, and specific signal transduction pathways are induced to adapt to environmental changes. In addition, microbial cells also have well-established repair mechanisms that protect their macromolecules against damages inflicted by environmental stresses. Oxidative, hyperosmotic, thermal, acid, and organic solvent stresses are significant in microbial fermentation. The overproduction of some metabolites as part of cell stress response can be of interest to biotechnology.

The main focus areas of this Special Issue are all possible applications of microbial stress response which can be of interest to biotechnology. Special attention will be paid to accumulation of various metabolites, such as polymers, carbohydrates, biosurfactants, pigments, sterols, lipids and unsaturated fatty acids, and many others. The other focus area is the influence of nutrition stress and use of waste lignocellulose materials, methanol, n-alkanes, starch, oils, and also other cheap carbon and nitrogen sources under the biorefinery conception. We are particularly interested in the biotechnological advantages of extremophiles. Any new knowledge connected with molecular stress mechanisms leading to improvement of biotechnological process is valuable. Additionally, manuscripts reporting possible ways of stress resistance mechanisms applications on the production of industrially important chemicals are appreciated. Growing interest in microbial applications in various fields coupled with significance of microbial stress metabolites in industrial applications as well as in health and dietary requirements has encouraged "hunting" for more suitable sources of these compounds.

Prof. Dr. Ivana Márová
Dr. Volha Shapaval
Guest Editors

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Keywords

Microbial biotechnology
Stress response
Biofuels
Biosurfactants
Single cell proteins
Single cell oils
Vitamins
Microbial polysaccharides
Polyhydroxyalkanoates
Bacteria
Yeasts
Fungi
Stress metabolites

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Published Papers (10 papers)

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Research

23 pages, 18123 KiB

Open AccessArticle

Use of Waste Substrates for the Lipid Production by Yeasts of the Genus Metschnikowia—Screening Study

by Andrea Němcová, Martin Szotkowski, Ota Samek, Linda Cagáňová, Matthias Sipiczki and Ivana Márová

Microorganisms 2021, 9(11), 2295; https://doi.org/10.3390/microorganisms9112295 - 4 Nov 2021

Cited by 5 | Viewed by 2643

Abstract

Oleogenic yeasts are characterized by the ability to accumulate increased amounts of lipids under certain conditions. These microbial lipids differ in their fatty acid composition, which allows them to be widely used in the biotechnology industry. The interest of biotechnologists is closely linked to the rising prices of fossil fuels in recent years. Their negative environmental impact is caused by significantly increased demand for biodiesel. The composition of microbial lipids is very similar to vegetable oils, which provides great potential for use in the production of biodiesel. In addition, some oleogenic microorganisms are capable of producing lipids with a high proportion of unsaturated fatty acids. The presented paper’s main aim was to study the production of lipids and lipid substances by yeasts of the genus Metschnikowia, to cultivate crude waste animal fat to study its utilization by yeasts, and to apply the idea of circular economy in the biotechnology of Metschnikowia yeasts. The work focuses on the influence of various stress factors in the cultivation process, such as reduced temperature or nutritional stress through the use of various waste substrates, together with manipulating the ratio of carbon and nitrogen sources in the medium. Yeast production properties were monitored by several instrumental techniques, including gas chromatography and Raman spectroscopy. The amount of lipids and in particular the fatty acid composition varied depending on the strains studied and the culture conditions used. The ability of yeast to produce significant amounts of unsaturated fatty acids was also demonstrated in the work. The most suitable substrate for lipid production was a medium containing glycerol, where the amount of accumulated lipids in the yeast M. pulcherrima 1232 was up to 36%. In our work, the crude animal fat was used for the production of high-value lipids, which to the best of our knowledge is a new result. Moreover, quantitative screening of lipase enzyme activity cultivated on animal fat substrate on selected yeasts of the genus Metschnikowia was performed. We found that for the yeast utilizing glycerol, animal fat seems to be an excellent source of carbon. Therefore, the yeast conversion of crude processed animal fat to value-added products is a valuable process for the biotechnology and food industry. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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21 pages, 4875 KiB

Open AccessArticle

Production of Enriched Sporidiobolus sp. Yeast Biomass Cultivated on Mixed Coffee Hydrolyzate and Fat/Oil Waste Materials

by Martin Szotkowski, Jiří Holub, Samuel Šimanský, Klára Hubačová, Dagmar Hladká, Andrea Němcová and Ivana Marová

Microorganisms 2021, 9(9), 1848; https://doi.org/10.3390/microorganisms9091848 - 31 Aug 2021

Cited by 5 | Viewed by 2264

Abstract

One of the most addressed topics today is the transfer from a linear model of economics to a model of circular economics. It is a discipline that seeks to eliminate waste produced by various industries. The food industry generates huge amounts of waste worldwide, particularly the coffee industry, and related industries produce millions of tons of waste a year. These wastes have potential utility in biotechnology, and in the production of energy, fuels, fertilizers and nutrients, using green techniques such as anaerobic digestion, co-digestion, composting, enzymatic action, and ultrasonic and hydrothermal carbonization. This work is focused on the biotechnological use of processed spent coffee grounds (SCG) and waste fat/oil materials by some Sporidiobolus sp. carotenogenic yeasts in the model of circular economics. The results show that selected yeast strains are able to grow on SCG hydrolysate and are resistant to antimicrobial compounds present in media. The most productive strain Sporidiobolus pararoseus CCY19-9-6 was chosen for bioreactor cultivation in media with a mixture of coffee lignocellulose fraction and some fat wastes. Sporidiobolus pararoseus CCY19-9-6 was able to produce more than 22 g/L of biomass in mixture of SCG hydrolysate and both coffee oil and frying oil. The combined waste substrates induced the production of lipidic metabolites, whereby the production of carotenoids exceeded 5 mg/g of dry biomass. On media with coffee oil, this strain produced high amounts of ubiquinone (8.265 ± 1.648 mg/g) and ergosterol (13.485 ± 1.275 mg/g). Overall, the results prove that a combination of waste substrates is a promising option for the production of carotenoid- and lipid-enriched yeast biomass. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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17 pages, 2205 KiB

Open AccessArticle

Stress Effect of Food Matrices on Viability of Probiotic Cells during Model Digestion

by Petra Matouskova, Julie Hoova, Petr Rysavka and Ivana Marova

Microorganisms 2021, 9(8), 1625; https://doi.org/10.3390/microorganisms9081625 - 30 Jul 2021

Cited by 17 | Viewed by 4067

Abstract

The aim of this study was to evaluate the influence of model (alcohol, sugar, salt, protein and acid) and real foods and beverages on the viability of probiotics during incubation and artificial digestion. Viability of monocultures Lactobacillus acidophilus CCM4833 and Bifidobacterium breve CCM7825T, and a commercial mixture of 9 probiotic bacterial strains, was tested by cultivation assay and flow cytometry. In model foods, the best viability was determined in the presence of 0.2 g/L glucose, 10% albumin and 10% ethanol. As the most suitable real food for probiotic survival, complex protein and carbohydrate substrates were found, such as beef broth, potato salad with pork, chicken with rice, chocolate spread, porridge and yoghurt. The best liquid was milk and meat broth, followed by Coca-Cola, beer and coffee. Viability of probiotics was higher when consumed with meals than with beverages only. Addition of prebiotics increased the viability of probiotics, especially in presence of instant and fast foods. Generally, the highest viability of probiotics during artificial digestion was observed in mixed culture in the presence of protein, sugar and fat, or their combination. The increase of cell viability observed in such foods during model digestion may further contribute to the positive effect of probiotics on human health. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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18 pages, 2035 KiB

Open AccessArticle

Rhodotorula kratochvilovae CCY 20-2-26—The Source of Multifunctional Metabolites

by Dana Byrtusová, Martin Szotkowski, Klára Kurowska, Volha Shapaval and Ivana Márová

Microorganisms 2021, 9(6), 1280; https://doi.org/10.3390/microorganisms9061280 - 11 Jun 2021

Cited by 15 | Viewed by 3423

Abstract

Multifunctional biomass is able to provide more than one valuable product, and thus, it is attractive in the field of microbial biotechnology due to its economic feasibility. Carotenogenic yeasts are effective microbial factories for the biosynthesis of a broad spectrum of biomolecules that can be used in the food and feed industry and the pharmaceutical industry, as well as a source of biofuels. In the study, we examined the effect of different nitrogen sources, carbon sources and CN ratios on the co-production of intracellular lipids, carotenoids, β–glucans and extracellular glycolipids. Yeast strain R. kratochvilovae CCY 20-2-26 was identified as the best co-producer of lipids (66.7 ± 1.5% of DCW), exoglycolipids (2.42 ± 0.08 g/L), β-glucan (11.33 ± 1.34% of DCW) and carotenoids (1.35 ± 0.11 mg/g), with a biomass content of 15.2 ± 0.8 g/L, by using the synthetic medium with potassium nitrate and mannose as a carbon source. It was shown that an increased C/N ratio positively affected the biomass yield and production of lipids and β-glucans. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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23 pages, 3458 KiB

Open AccessArticle

Bioreactor Co-Cultivation of High Lipid and Carotenoid Producing Yeast Rhodotorula kratochvilovae and Several Microalgae under Stress

by Martin Szotkowski, Jiří Holub, Samuel Šimanský, Klára Hubačová, Pavlína Sikorová, Veronika Mariničová, Andrea Němcová and Ivana Márová

Microorganisms 2021, 9(6), 1160; https://doi.org/10.3390/microorganisms9061160 - 28 May 2021

Cited by 11 | Viewed by 3731

Abstract

The co-cultivation of red yeasts and microalgae works with the idea of the natural transport of gases. The microalgae produce oxygen, which stimulates yeast growth, while CO₂ produced by yeast is beneficial for algae growth. Both microorganisms can then produce lipids. The present pilot study aimed to evaluate the ability of selected microalgae and carotenogenic yeast strains to grow and metabolize in co-culture. The effect of media composition on growth and metabolic activity of red yeast strains was assessed simultaneously with microalgae mixotrophy. Cultivation was transferred from small-scale co-cultivation in Erlenmeyer flasks to aerated bottles with different inoculation ratios and, finally, to a 3L bioreactor. Among red yeasts, the strain R. kratochvilovae CCY 20-2-26 was selected because of the highest biomass production on BBM medium. Glycerol is a more suitable carbon source in the BBM medium and urea was proposed as a compromise. From the tested microalgae, Desmodesmus sp. were found as the most suitable for co-cultivations with R. kratochvilovae. In all co-cultures, linear biomass growth was found (144 h), and the yield was in the range of 8.78–11.12 g/L of dry biomass. Lipids increased to a final value of 29.62–31.61%. The FA profile was quite stable with the UFA portion at about 80%. Around 1.98–2.49 mg/g CDW of carotenoids with torularhodine as the major pigment were produced, ubiquinone production reached 5.41–6.09 mg/g, and ergosterol yield was 6.69 mg/g. Chlorophyll production was very low at 2.11 mg/g. Pilot experiments have confirmed that carotenogenic yeasts and microalgae are capable of symbiotic co-existence with a positive impact om biomass growth and lipid metabolites yields. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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12 pages, 1700 KiB

Open AccessArticle

Glucose-Limited Fed-Batch Cultivation Strategy to Mimic Large-Scale Effects in Escherichia coli Linked to Accumulation of Non-Canonical Branched-Chain Amino Acids by Combination of Pyruvate Pulses and Dissolved Oxygen Limitation

by Ángel Córcoles García, Peter Hauptmann and Peter Neubauer

Microorganisms 2021, 9(6), 1110; https://doi.org/10.3390/microorganisms9061110 - 21 May 2021

Cited by 3 | Viewed by 3480

Abstract

Insufficient mixing in large-scale bioreactors provokes gradient zones of substrate, dissolved oxygen (DO), pH, and other parameters. E. coli responds to a high glucose, low oxygen feeding zone with the accumulation of mixed acid fermentation products, especially formate, but also with the synthesis of non-canonical amino acids, such as norvaline, norleucine and β-methylnorleucine. These amino acids can be mis-incorporated into recombinant products, which causes a problem for pharmaceutical production whose solution is not trivial. While these effects can also be observed in scale down bioreactor systems, these are challenging to operate. Especially the high-throughput screening of clone libraries is not easy, as fed-batch cultivations would need to be controlled via repeated glucose pulses with simultaneous oxygen limitation, as has been demonstrated in well controlled robotic systems. Here we show that not only glucose pulses in combination with oxygen limitation can provoke the synthesis of these non-canonical branched-chain amino acids (ncBCAA), but also that pyruvate pulses produce the same effect. Therefore, we combined the enzyme-based glucose delivery method Enbase^® in a PALL24 mini-bioreactor system and combined repeated pyruvate pulses with simultaneous reduction of the aeration rate. These cultivation conditions produced an increase in the non-canonical branched chain amino acids norvaline and norleucine in both the intracellular soluble protein and inclusion body fractions with mini-proinsulin as an example product, and this effect was verified in a 15 L stirred tank bioreactor (STR). To our opinion this cultivation strategy is easy to apply for the screening of strain libraries under standard laboratory conditions if no complex robotic and well controlled parallel cultivation devices are available. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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13 pages, 1349 KiB

Open AccessArticle

The First Insight into Polyhydroxyalkanoates Accumulation in Multi-Extremophilic Rubrobacter xylanophilus and Rubrobacter spartanus

by Xenie Kouřilová, Jana Schwarzerová, Iva Pernicová, Karel Sedlář, Kateřina Mrázová, Vladislav Krzyžánek, Jana Nebesářová and Stanislav Obruča

Microorganisms 2021, 9(5), 909; https://doi.org/10.3390/microorganisms9050909 - 24 Apr 2021

Cited by 30 | Viewed by 3440

Abstract

Actinobacteria belonging to the genus Rubrobacter are known for their multi-extremophilic growth conditions—they are highly radiation-resistant, halotolerant, thermotolerant or even thermophilic. This work demonstrates that the members of the genus are capable of accumulating polyhydroxyalkanoates (PHA) since PHA-related genes are widely distributed among Rubrobacter spp. whose complete genome sequences are available in public databases. Interestingly, all Rubrobacter strains possess both class I and class III synthases (PhaC). We have experimentally investigated the PHA accumulation in two thermophilic species, R. xylanophilus and R. spartanus. The PHA content in both strains reached up to 50% of the cell dry mass, both bacteria were able to accumulate PHA consisting of 3-hydroxybutyrate and 3-hydroxyvalerate monomeric units, none other monomers were incorporated into the polymer chain. The capability of PHA accumulation likely contributes to the multi-extremophilic characteristics since it is known that PHA substantially enhances the stress robustness of bacteria. Hence, PHA can be considered as extremolytes enabling adaptation to extreme conditions. Furthermore, due to the high PHA content in biomass, a wide range of utilizable substrates, Gram-stain positivity, and thermophilic features, the Rubrobacter species, in particular Rubrobacter xylanophilus, could be also interesting candidates for industrial production of PHA within the concept of Next-Generation Industrial Biotechnology. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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14 pages, 8031 KiB

Open AccessArticle

Pigment Production Improvement in Rhodotorula mucilaginosa AJB01 Using Design of Experiments

by Alejandra Garcia-Cortes, Julián Andres Garcia-Vásquez, Yani Aranguren and Mauricio Ramirez-Castrillon

Microorganisms 2021, 9(2), 387; https://doi.org/10.3390/microorganisms9020387 - 14 Feb 2021

Cited by 20 | Viewed by 5170

Abstract

The discovery of biopigments has received considerable attention from the industrial sector, mainly for potential applications as novel molecules with biological activity, in cosmetics or if aquaculture food supplements. The main objective of this study was to increase the production of carotenoid pigments in a naturally pigmented yeast by subjecting the yeast to various cellular stresses using design of experiments. The fungal strain Rhodotorula mucilaginosa AJB01 was isolated from a food sample collected in Barranquilla, Colombia, and one of the pigments produced was β-carotene. This strain was subjected to various stress conditions, including osmotic stress using different salts, physical stress by ultraviolet (UV) light, and light stress using different photoperiods. The optimal growth conditions for carotenoid production were determined to be 1 min of UV light, 0.5 mg/L of magnesium sulfate, and an 18:6 h light/dark period, which resulted in a carotenoid yield of 118.3 µg of carotenoid per gram of yeast. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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19 pages, 6359 KiB

Open AccessArticle

The Use of Raman Spectroscopy to Monitor Metabolic Changes in Stressed Metschnikowia sp. Yeasts

by Andrea Němcová, Dominika Gonová, Ota Samek, Matthias Sipiczki, Emilia Breierová and Ivana Márová

Microorganisms 2021, 9(2), 277; https://doi.org/10.3390/microorganisms9020277 - 29 Jan 2021

Cited by 8 | Viewed by 3471

Abstract

Raman spectroscopy is a universal method designed for the analysis of a wide range of physical, chemical and biological systems or various surfaces. This technique is suitable to monitor various components of cells, tissues or microorganisms. The advantages include very fast non-contact and non-destructive analysis and no or minimal need for sample treatment. The yeasts Metschnikowia can be considered as industrially usable producers of pulcherrimin or single-cell lipids, depending on cultivation conditions and external stress. In the present study, Raman spectroscopy was used as an effective tool to identify both pulcherrimin and lipids in single yeast cells. The analysis of pulcherrimin is very demanding; so far, there is no optimal procedure to analyze or identify this pigment. Based on results, the strong dependence of pulcherrimin production on the ferric ion concentration was found with the highest yield in media containing 0.1 g/L iron. Further, production of lipids in Metschnikowia cells was studied at different temperatures and C:N ratios, using Raman spectroscopy to follow fatty acids composition, under different regimes, by monitoring the iodine number. The results of Raman spectroscopy were comparable with the fatty acid analysis obtained by gas chromatography. This study therefore supported use of Raman spectroscopy for biotechnological applications as a simple tool in the identification and analysis both the pulcherrimin and microbial lipids. This method provides a quick and relatively accurate estimation of targeted metabolites with minimal sample modification and allows to monitor metabolic changes over time of cultivation. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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19 pages, 2627 KiB

Open AccessArticle

Revealing the Potential of Lipid and β-Glucans Coproduction in Basidiomycetes Yeast

by Dana Byrtusová, Volha Shapaval, Jiří Holub, Samuel Šimanský, Marek Rapta, Martin Szotkowski, Achim Kohler and Ivana Márová

Microorganisms 2020, 8(7), 1034; https://doi.org/10.3390/microorganisms8071034 - 13 Jul 2020

Cited by 23 | Viewed by 3328

Abstract

Beta (β)–glucans are polysaccharides composed of D-glucose monomers. Nowadays, β-glucans are gaining attention due to their attractive immunomodulatory biological activities, which can be utilized in pharmaceutical or food supplementation industries. Some carotenogenic Basidiomycetes yeasts, previously explored for lipid and carotenoid coproduction, could potentially coproduce a significant amount of β–glucans. In the present study, we screened eleven Basidiomycetes for the coproduction of lipids and β–glucans. We examined the effect of four different C/N ratios and eight different osmolarity conditions on the coproduction of lipids and β–glucans. A high-throughput screening approach employing microcultivation in microtiter plates, Fourier Transform Infrared (FTIR) spectroscopy and reference analysis was utilized in the study. Yeast strains C. infirmominiatum CCY 17-18-4 and R. kratochvilovae CCY 20-2-26 were identified as the best coproducers of lipids and β-glucans. In addition, C. infirmominiatum CCY 17-18-4, R. kratochvilovae CCY 20-2-26 and P. rhodozyma CCY 77-1-1 were identified as the best alternative producers of β-glucans. Increased C/N ratio led to increased biomass, lipid and β-glucans production for several yeast strains. Increased osmolarity had a negative effect on biomass and lipid production while the β-glucan production was positively affected. Full article

(This article belongs to the Special Issue Microbial Stress Response as a Tool for Biotechnology)

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