Publications by authors named "Alexander Mathys"

40 Publications

Transfer of Lauric and Myristic Acid from Black Soldier Fly Larval Lipids to Egg Yolk Lipids of Hens Is Low.

Lipids 2021 Apr 22. Epub 2021 Apr 22.

ETH Zurich, Institute of Agricultural Sciences, Animal Nutrition, Zurich, Universitaetstrasse 2, 8092, Switzerland.

Implementing insects, such as the black soldier fly larvae (BSFL), as animal feed commonly includes the previous removal of substantial amounts of fat. This fat may represent an as yet underutilized energy source for livestock. However, transfer of lauric and myristic acid, prevalent in BSFL fat and undesired in human nutrition, into animal-source foods like eggs may limit its implementation. To quantify this, a laying hen experiment was performed comprising five different diets (10 hens/diet). These were a control diet with soybean oil and meal and a second diet with soybean oil but with partially defatted BSFL meal as protein source. The other three diets were based on different combinations of partially defatted BSFL meal and fat obtained by two different production methods. Lauric acid made up half of the BSFL fat from both origins. Both BSFL fats also contained substantial amounts of myristic and palmitic acid. However, in the insect-based diets, the net transfer from diet to egg yolk was less than 1% for lauric acid, whereas the net transfer for myristic and palmitic acid was about 30% and 100%, respectively. The net transfer did not vary between BSFL originating from production on different larval feeding substrates. The results illustrate that hens are able to metabolize or elongate very large proportions of ingested lauric acid and myristic acid, which are predominant in the BSFL lipids (together accounting for as much as 37 mol%), such that they collectively account for less than 3.5 mol% of egg yolk fatty acids.
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http://dx.doi.org/10.1002/lipd.12304DOI Listing
April 2021

Automated Online Flow Cytometry Advances Microalgal Ecosystem Management as , High-Temporal Resolution Monitoring Tool.

Front Bioeng Biotechnol 2021 23;9:642671. Epub 2021 Mar 23.

Sustainable Food Processing Laboratory, Institute of Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland.

Microalgae are emerging as a next-generation biotechnological production system in the pharmaceutical, biofuel, and food domain. The economization of microalgal biorefineries remains a main target, where culture contamination and prokaryotic upsurge are main bottlenecks to impair culture stability, reproducibility, and consequently productivity. Automated online flow cytometry (FCM) is gaining momentum as bioprocess optimization tool, as it allows for spatial and temporal landscaping, real-time investigations of rapid microbial processes, and the assessment of intrinsic cell features. So far, automated online FCM has not been applied to microalgal ecosystems but poses a powerful technology for improving the feasibility of microalgal feedstock production through , real-time, high-temporal resolution monitoring. The study lays the foundations for an application of automated online FCM implying far-reaching applications to impel and facilitate the implementation of innovations targeting at microalgal bioprocesses optimization. It shows that emissions collected on the FL1/FL3 fluorescent channels, harnessing nucleic acid staining and chlorophyll autofluorescence, enable a simultaneous assessment (quantitative and diversity-related) of prokaryotes and industrially relevant phototrophic in mixed ecosystems of different complexity over a broad concentration range (2.2-1,002.4 cells ⋅μL). Automated online FCM combined with data analysis relying on phenotypic fingerprinting poses a powerful tool for quantitative and diversity-related population dynamics monitoring. Quantitative data assessment showed that prokaryotic growth phases in engineered and natural ecosystems were characterized by different growth speeds and distinct peaks. Diversity-related population monitoring based on phenotypic fingerprinting indicated that prokaryotic upsurge in mixed cultures was governed by the dominance of single prokaryotic species. Automated online FCM is a powerful tool for microalgal bioprocess optimization owing to its adaptability to myriad phenotypic assays and its compatibility with various cultivation systems. This allows advancing bioprocesses associated with both microalgal biomass and compound production. Hence, automated online FCM poses a viable tool with applications across multiple domains within the biobased sector relying on single cell-based value chains.
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http://dx.doi.org/10.3389/fbioe.2021.642671DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8023406PMC
March 2021

Isolation, stability, and characteristics of high-pressure superdormant Bacillus subtilis spores.

Int J Food Microbiol 2021 Apr 11;343:109088. Epub 2021 Feb 11.

Sustainable Food Processing Laboratory, Institute of Food, Nutrition and Health, Department of Health Science and Technology, ETH Zurich, Zurich, Switzerland. Electronic address:

Bacterial spores are a major challenge in industrial decontamination processes owing to their extreme resistance. High-pressure (HP) of 150 MPa at 37 °C can trigger the germination of spores, making them lose their extreme resistance. Once their resistance is lost, germinated spores can easily be inactivated by a mild decontamination step. The implementation of this gentle germination-inactivation strategy is hindered by the presence of a subpopulation of so-called high-pressure superdormant (HPSD) spores, which resist germination or germinate only very slowly in response to HP. It is essential to understand the properties of HPSD spores and the underlying causes of superdormancy to tackle superdormant spores and further develop germination-inactivation strategies involving HP. This study investigated factors influencing the prevalence of HPSD spores and successfully isolated them by combining buoyant density centrifugation and fluorescence-activated cell sorting, which allowed further characterisation of HPSD spores for the first time. The prevalence of HPSD spores was shown to be strongly dependent on the HP dwell time, with increasing treatment times reducing their prevalence. Spore mutants lacking major germinant receptors further showed a highly increased prevalence of HPSD spores; 93% of the spores remained dormant even after a prolonged HP dwell time of 40 min. In contrast to nutrient germination, sublethal heat treatment of 75 °C for 30 min prior to pressure treatment did not induce spore activation and increase germination. The isolated HPSD spores did not show visible structural differences compared to the initial dormant spores when investigated with transmission electron microscopy. Re-sporulated HPSD spores showed similar germination capacity compared to the initial dormant spores, indicating that HPSD spores are most likely not genetically different from the rest of the population. Moreover, the majority of HPSD spores germinated when exposed a second time to the same germination treatment; however, the germination capacity was lower than that of the initial population. The fact that the majority of spores lost superdormancy when exposed a second time to the same trigger makes it unlikely that there is one factor that determines whether a spore germinates with a certain HP treatment or not. Instead, it seems possible that there are other reversible or cumulative causes. This study investigated the factors influencing spore HP superdormancy to improve the understanding of HPSD spores with regard to their stability, germination capacity, and potential underlying causes of spore HP superdormancy. This knowledge will contribute to the development of HP-based germination-inactivation strategies for gentle but effective spore control.
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http://dx.doi.org/10.1016/j.ijfoodmicro.2021.109088DOI Listing
April 2021

Biochemical and Morphological Characterization of Heterotrophic and Cell Walls.

J Agric Food Chem 2021 Feb 11;69(7):2226-2235. Epub 2021 Feb 11.

Laboratory of Sustainable Food Processing, ETH Zürich, Schmelzbergstrasse 9, 8092 Zürich, Switzerland.

Microalgae are attractive for the food and cosmetic industries because of their nutrient composition. However, the bioaccessibility and extractability of nutrients in microalgae are limited by the rigid and indigestible cell wall. The goal of this study is to explore the cell wall polysaccharides (CWPSs) composition and morphology in heterotrophic and biomasses during growth. Our results showed that glucose was the major component of CWPSs and exopolysaccharides in . CWPSs have a similar sugar profile in exponential and stationary phases, essentially composed of rhamnose and galactose. cell wall thickness increased from 82 nm in the exponential phase to 114 nm in the stationary phase and consisted of two main layers. cell wall was 133 nm thick and composed of several membranes surrounding thecal plates. Understanding of the microalgae cell wall helps developing a more efficient and targeted biorefinery approach.
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http://dx.doi.org/10.1021/acs.jafc.0c05032DOI Listing
February 2021

Identification of Bacteria in Two Food Waste Black Soldier Fly Larvae Rearing Residues.

Front Microbiol 2020 23;11:582867. Epub 2020 Nov 23.

Sustainable Food Processing Laboratory, Department of Health Science and Technology, Institute of Food, Nutrition and Health, ETH Zürich, Zurich, Switzerland.

Significant economic, environmental, and social impacts are associated with the avoidable disposal of foods worldwide. Mass-rearing of black soldier fly () larvae using organic wastes and food- and agro-industry side products is promising for recycling resources within the food system. One current challenge of this approach is ensuring a reliable and high conversion performance of larvae with inherently variable substrates. Research has been devoted to increasing rearing performance by optimizing substrate nutrient contents and ratios, while the potential of the substrate and larval gut microbiota to increase rearing performance remains untapped. Since previous research has focused on gut microbiota, here, we describe bacterial dynamics in the residue (i.e., the mixture of frass and substrate) of black soldier fly larvae reared on two food wastes (i.e., canteen and household waste). To identify members of the substrate and residue microbiota, potentially associated with rearing performance, bacterial dynamics were also studied in the canteen waste without larvae, and after inactivation by irradiation of the initial microbiota in canteen waste. The food waste substrates had similar microbiota; both were dominated by common lactic acid bacteria. Inactivation of the canteen waste microbiota, which was dominated by , , and , decreased the levels of all rearing performance indicators by 31-46% relative to canteen waste with the native microbiota. In both food waste substrates, larval rearing decreased the bacterial richness and changed the physicochemical residue properties and composition over the rearing period of 12 days, and typical members of the larval intestinal microbiota (i.e., , , , and became more abundant, suggesting their transfer into the residue through excretions. Future studies should isolate members of these taxa and elucidate their true potential to influence black soldier fly mass-rearing performance.
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http://dx.doi.org/10.3389/fmicb.2020.582867DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719680PMC
November 2020

Articulating the effect of food systems innovation on the Sustainable Development Goals.

Lancet Planet Health 2021 01 9;5(1):e50-e62. Epub 2020 Dec 9.

International Institute for Applied Systems Analysis (IIASA), Laxenburg, Austria.

Food system innovations will be instrumental to achieving multiple Sustainable Development Goals (SDGs). However, major innovation breakthroughs can trigger profound and disruptive changes, leading to simultaneous and interlinked reconfigurations of multiple parts of the global food system. The emergence of new technologies or social solutions, therefore, have very different impact profiles, with favourable consequences for some SDGs and unintended adverse side-effects for others. Stand-alone innovations seldom achieve positive outcomes over multiple sustainability dimensions. Instead, they should be embedded as part of systemic changes that facilitate the implementation of the SDGs. Emerging trade-offs need to be intentionally addressed to achieve true sustainability, particularly those involving social aspects like inequality in its many forms, social justice, and strong institutions, which remain challenging. Trade-offs with undesirable consequences are manageable through the development of well planned transition pathways, careful monitoring of key indicators, and through the implementation of transparent science targets at the local level.
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http://dx.doi.org/10.1016/S2542-5196(20)30277-1DOI Listing
January 2021

Biochemical and Nutritional Evaluation of and Biomasses Relevant for Food Application.

Front Nutr 2020 30;7:565996. Epub 2020 Sep 30.

Laboratory of Sustainable Food Processing, ETH Zurich, Swiss Federal Institute of Technology, Zurich, Switzerland.

Microalgae are a source of potentially healthy and sustainable nutrients. However, the bioaccessibility of these nutrients remains uncertain. In this study, we analyzed the biomass composition of five commercial and strains, and heterotrophically cultivated in our laboratory. Protein accounted for 65 ± 3% (w w) dry matter (DM) in all biomasses, except for the lab-grown that contained 20% (w w) DM protein. The fatty acids content was comparable and ranged between 7 and 10% (w w) DM. Most of the biomasses had a ω6-polyunsaturated fatty acids (PUFAs)/ω3-PUFAs ratio <4, as recommended by nutritional experts. A recently published harmonized protocol for digestion was used to evaluate fatty acids and protein bioaccessibilities. Protein bioaccessibility ranged between 60 and 74% for commercial and biomasses and was 43% for the lab-grown . Fatty acids bioaccessibility was <7% in commercial biomasses and 19% in the lab-grown . Taken together, the results show that microalgae are promising sources of bioaccessible protein. The limited fatty acids bioaccessibility indicates the need for alternative upstream and downstream production strategies.
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http://dx.doi.org/10.3389/fnut.2020.565996DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7557355PMC
September 2020

Effect of Arthrospira platensis microalgae protein purification on emulsification mechanism and efficiency.

J Colloid Interface Sci 2021 Feb 24;584:344-353. Epub 2020 Sep 24.

ETH Zurich, Department of Health Science and Technology, Institute of Food, Nutrition and Health, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, 8092 Zurich, Switzerland. Electronic address:

In light of environmental concerns and changing consumer demands, efforts are increasing to replace frequently used animal-based emulsifiers. We demonstrate the interfacial network formation and emulsifying potential of Arthrospira platensis protein extracts and hypothesize a mechanistic change upon progressing purification. A microalgae suspension of A. platensis powder in phosphate buffer solution (pH 7, 0.1 M) was homogenized and insoluble components separated by centrifugation. Proteins were precipitated at the identified isoelectric point at pH 3.5 and diafiltrated. In interfacial shear rheology measurements, the build-up of an interfacial viscoelastic network was faster and final network strength increased with the degree of purification. It is suggested that isolated A. platensis proteins rapidly form an interconnected protein layer while coextracted surfactants impede protein adsorption for crude and soluble extracts. Emulsions with 20 vol % medium chain triglycerides (MCT) oil could be formed with all extracts of different degrees of purification. Normalized by protein concentration, smaller droplets could be stabilized with the isolated fractions. For potential applications in food, pharma and cosmetic product categories, the enhanced functionality has to be balanced against the loss in biomass while purifying microalgae proteins or other alternative single cell proteins.
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http://dx.doi.org/10.1016/j.jcis.2020.09.067DOI Listing
February 2021

Nanosecond pulsed electric field processing of microalgae based biorefineries governs growth promotion or selective inactivation based on underlying microbial ecosystems.

Bioresour Technol 2021 Jan 24;319:124173. Epub 2020 Sep 24.

Swiss Federal Institute of Technology (ETH), Zurich, Institute of Food, Nutrition and Health, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, Zurich 8092, Switzerland. Electronic address:

Nanosecond pulsed electric field treatment (nsPEF) is a technology-driven, resource-efficient approach fostering microalgae biorefineries for transforming them into economically viable scenarios. A processing window of 100 ns, 7 Hz, and 10 kV cm significantly leveraged phototrophic Chlorella vulgaris and bacterial counts up to + 50.1 ± 12.2% and + 77.0 ± 37.4%, respectively (n = 4; p < 0.05) in non-axenic cultures. Applying the same processing window decreased C. vulgaris (-17.1 ± 13.8%) and prokaryotic (-82.7 ± 14.6%) counts owing to alterations in the prokaryotic community diversity. Principle coordinate analysis of prokaryotic phenotypic fingerprints indicated that phenotype or metabolism related diversity changes in the prokaryotic community affected the treatment outcome. The study fosters the upsurge of industrial-scale nsPEF realization and the economic viability of microalgae biorefineries through improved process understanding and thus control. It perpetuates nsPEF applicability for microalgae feedstock production and several other applications within single-cell biorefineries in the bio-based domain.
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http://dx.doi.org/10.1016/j.biortech.2020.124173DOI Listing
January 2021

Novel Experimental Methods for the Investigation of Hermetia illucens (Diptera: Stratiomyidae) Larvae.

J Insect Sci 2020 May;20(3)

ETH Zurich, Institute of Agricultural Sciences, Zurich, Switzerland.

Large-scale insect rearing for food and feed production can be improved by understanding diet digestion and host-microbe interactions. To examine these processes in black soldier fly (Hermetia illucens L.; Diptera: Stratiomyidae) larvae, two protocols were developed. Protocol 1 describes a method to produce viable, sterile black soldier fly larvae and a gentle method for diet sterilization. Sterile black soldier fly larvae can be used to study the diverse role of microbes in larval development. Nutrient requirements of sterile black soldier fly larvae are met only through diet. Viable sterile black soldier fly larvae were consistently generated using a four-step treatment with alternating immersions of eggs for 2 min each in ethanol (70%) and sodium hypochlorite (0.6%), over two cycles. A nonthermal method of diet sterilization, namely high-energy electron beam (HEEB) treatment, was introduced. Subsequently, growth of sterile black soldier fly larvae was observed on the HEEB-treated diets (40, 60, and 40% of replicates with poultry feed, liver pie, and an artificial diet, respectively) but not on autoclaved diets. In Protocol 2, we propose a novel method to collect frass from individual larvae. We then measured the metabolites in frass, using high-pressure liquid chromatography. Results on metabolites confirmed the influence of digestion. For instance, succinate increased from 1 to 2 and 7 μmol/g sample from diet to gut homogenate and frass, respectively. The collection method is a promising tool to estimate the diet and nutrient requirements of black soldier fly larvae, thus increasing the performance and reliability of black soldier fly larvae rearing. We discuss in detail the possible applications and limitations of our methods in black soldier fly larvae research.
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http://dx.doi.org/10.1093/jisesa/ieaa057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7320877PMC
May 2020

Estimating black soldier fly larvae biowaste conversion performance by simulation of midgut digestion.

Waste Manag 2020 Jul 1;112:40-51. Epub 2020 Jun 1.

ETH Zurich: Swiss Federal Institute of Technology Zurich, Institute of Food, Nutrition and Health, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, 8092 Zurich, Switzerland. Electronic address:

Black soldier fly larvae treatment is an emerging technology for the conversion of biowaste into potentially more sustainable and marketable high-value products, according to circular economy principles. Unknown or variable performance for different biowastes is currently one challenge that prohibits the global technology up-scaling. This study describes simulated midgut digestion for black soldier fly larvae to estimate biowaste conversion performance. Before simulation, the unknown biowaste residence time in the three midgut regions was determined on three diets varying in protein and non-fiber carbohydrate content. For the static in vitro model, diet residence times of 15 min, 45 min, and 90 min were used for the anterior, middle, and posterior midgut region, respectively. The model was validated by comparing the ranking of diets based on in vitro digestion products to the ranking found in in vivo feeding experiments. Four artificial diets and five biowastes were digested using the model, and diet digestibility and supernatant nutrient contents were determined. This approach was able to distinguish broadly the worst and best performing rearing diets. However, for some of the diets, the performance estimated based on in vitro results did not match with the results of the feeding experiments. Future studies should try to establish a stronger correlation by considering fly larvae nutrient requirements, hemicellulose digestion, and the diet/gut microbiota. In vitro digestion models could be a powerful tool for academia and industry to increase conversion performance of biowastes with black soldier fly larvae.
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http://dx.doi.org/10.1016/j.wasman.2020.05.026DOI Listing
July 2020

Characterization of Chlorella vulgaris (Trebouxiophyceae) associated microbial communities.

J Phycol 2020 10 22;56(5):1308-1322. Epub 2020 Jun 22.

Laboratory of Sustainable Food Processing, Institute of Food, Nutrition and Health, Swiss Federal Institute of Technology (ETH), Schmelzbergstrasse 9, 8092, Zürich, Switzerland.

Microalgae exhibit extensive potential for counteracting imminent challenges in the nutraceutical, pharmaceutical, and biomaterial sectors, but lack economic viability. Biotechnological systems for contamination control could advance the economic viability of microalgal feedstock, but the selection of suitable strains that sustainably promote microalgal productivity remains challenging. In this study, total diversity in phototrophic Chlorella vulgaris cultures was assessed by amplicon sequencing comparing cultures subjected to five different cultivation conditions. Overall, 12 eukaryotic and 53 prokaryotic taxa were identified; Alphaproteobacteria (36.7%) dominated the prokaryotic and C. vulgaris (97.2%) the eukaryotic community. Despite altering cultivation conditions, 2 eukaryotic and 40 prokaryotic taxa remained stably associated with C. vulgaris; diversity between systems did not significantly differ (P > 0.05). Among those, 20 cultivable taxa were isolated and identified by 16S rDNA sequencing. Subsequently, controlled co-cultures were investigated showing stable associations of C. vulgaris with Sphingopyxis sp. and Pseudomonas sp.. Out-competition of C. vulgaris due to ammonium or phosphate limitation was not observed, despite significantly elevated growth of Sphingopyxis sp. and Tistrella sp.. (P < 0.05). Nevertheless, C. vulgaris growth was impaired by Tistrella sp.. Hence, the study provides a selection of stable indigenous prokaryotes and eukaryotes for artificially tailoring microbial biocenoses. Following a bottom-up approach, it provides a base for controlled co-cultures and thus the establishment of even more complex biocenoses using interkingdom assemblages. Such assemblages can benefit from functional richness for improved nutrient utilization, as well as bacterial load control, which can enhance microalgal feedstock production through improved culture stability and productivity.
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http://dx.doi.org/10.1111/jpy.13026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7687158PMC
October 2020

Time-temperature-resolved functional and structural changes of phycocyanin extracted from Arthrospira platensis/Spirulina.

Food Chem 2020 Jun 6;316:126374. Epub 2020 Feb 6.

ETH Zurich, Department of Health Science and Technology, Institute of Food, Nutrition and Health, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, 8092 Zurich, Switzerland. Electronic address:

Arthrospira platensis, commonly known as Spirulina, gains increasing importance as alternative protein source for food production and biotechnological systems. A promising area is functional high-value algae extracts, rich in phycocyanin, a protein-pigment complex derived from A. platensis. This complex has proven functionality as the only natural blue colorant, fluorescent marker and therapeutic agent. The structure-function relationship is heat sensitive, making thermal processing in its production and its subsequent application a crucial aspect. In continuous high-temperature short-time treatments, it was shown how a purified phycocyanin (mixture of allophycocyanin and c-phycocyanin) disassembled and denatured between 50 and 70 °C. Three characteristic transition temperatures were allocated to specific quaternary aggregates. In contrast to sequential chemical denaturation, phycocyanin's chromophore and protein structure were simultaneously affected by thermal processing. Through a functionality assessment, the findings help optimize the efficiency of raw material usage by defining a processing window, enabling targeted process control resulting in desired product properties.
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http://dx.doi.org/10.1016/j.foodchem.2020.126374DOI Listing
June 2020

Flow Cytometry Combined With Single Cell Sorting to Study Heterogeneous Germination of Spores Under High Pressure.

Front Microbiol 2019 21;10:3118. Epub 2020 Jan 21.

Sustainable Food Processing Laboratory, Institute of Food, Nutrition and Health, Department of Health Science and Technology, ETH Zürich, Zurich, Switzerland.

Isostatic high pressure (HP) of 150 MPa can trigger the germination of bacterial spores, making them lose their extreme resistance to stress factors, and increasing their susceptibility to milder inactivation strategies. However, germination response of spores within a population is very heterogeneous, and tools are needed to study this heterogeneity. Here, classical methods were combined with more recent and powerful techniques such as flow cytometry (FCM) and fluorescence activated cell sorting (FACS) to investigate spore germination behavior under HP. spores were treated with HP at 150 MPa and 37°C, stained with SYTO16 and PI, and analyzed via FCM. Four sub-populations were detected. These sub-populations were for the first time isolated on single cell level using FACS and characterized in terms of their heat resistance (80°C, 10 min) and cultivability in a nutrient-rich environment. The four isolated sub-populations were found to include (1) heat-resistant and mostly cultivable superdormant spores, i.e., spores that remained dormant after this specific HP treatment, (2) heat-sensitive and cultivable germinated spores, (3) heat-sensitive and partially-cultivable germinated spores, and (4) membrane-compromised cells with barely detectable cultivability. Of particular interest was the physiological state of the third sub-population, which was previously referred to as "unknown". Moreover, the kinetic transitions between different physiological states were characterized. After less than 10 min of HP treatment, the majority of spores germinated and ended up in a sublethally damaged stage. HP treatment at 150 MPa and 37°C did not cause inactivation of all geminated spores, suggesting that subsequent inactivation strategies such as mild heat inactivation or other inactivation techniques are necessary to control spores in food. This study validated FCM as a powerful technique to investigate the heterogeneous behavior of spores under HP, and provided a pipeline using FACS for isolation of different sub-populations and subsequent characterization to understand their physiological states.
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http://dx.doi.org/10.3389/fmicb.2019.03118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6985370PMC
January 2020

Role of DNA repair in Bacillus subtilis spore resistance to high energy and low energy electron beam treatments.

Food Microbiol 2020 May 30;87:103353. Epub 2019 Oct 30.

Sustainable Food Processing Laboratory, Institute of Food, Nutrition and Health, Department of Health Science and Technology, ETH Zurich, Zurich, Switzerland. Electronic address:

Bacillus subtilis spore inactivation mechanisms under low energy electron beam (LEEB) and high energy electron beam (HEEB) treatment were investigated using seven mutants lacking specific DNA repair mechanisms. The results showed that most of the DNA repair-deficient mutants, including ΔrecA, ΔKu ΔligD, Δexo Δnfo, ΔuvrAB and ΔsbcDC, had reduced resistances towards electron beam (EB) treatments at all investigated energy levels (80 keV, 200 keV and 10 MeV) compared to their wild type. This result suggested DNA damage was induced during EB treatments. The mutant lacking recA showed the lowest resistance, followed by the mutant lacking Ku and ligD. These findings indicated that recA, Ku and ligD and their associated DNA repair mechanisms, namely, homologous recombination and non-homologous end joining, play important roles in spore survival under EB treatment. Furthermore, exoA, nfo, uvrAB, splB, polY1 and polY2, which are involved in nucleotide damage repair/removal, showed different levels of effects on spore resistance under EB treatment. Finally, the results suggested that HEEB and LEEB inactivate B. subtilis spores through similar mechanisms. This research will provide a better understanding of how EB technologies inactivate B. subtilis spores and will contribute to the application of these technologies as a non-thermal, gentle spore control approach.
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http://dx.doi.org/10.1016/j.fm.2019.103353DOI Listing
May 2020

Endospore Inactivation by Emerging Technologies: A Review of Target Structures and Inactivation Mechanisms.

Annu Rev Food Sci Technol 2020 03 24;11:255-274. Epub 2019 Dec 24.

Sustainable Food Processing Laboratory, Department of Health Science and Technology, ETH Zurich, CH-8092 Zurich, Switzerland; email:

Recent developments in preservation technologies allow for the delivery of food with nutritional value and superior taste. Of special interest are low-acid, shelf-stable foods in which the complete control or inactivation of bacterial endospores is the crucial step to ensure consumer safety. Relevant preservation methods can be classified into physicochemical or physical hurdles, and the latter can be subclassified into thermal and nonthermal processes. The underlying inactivation mechanisms for each of these physicochemical or physical processes impact different morphological or molecular structures essential for spore germination and integrity in the dormant state. This review provides an overview of distinct endospore defense mechanisms that affect emerging physical hurdles as well as which technologies address these mechanisms. The physical spore-inactivation technologies considered include thermal, dynamic, and isostatic high pressure and electromagnetic technologies, such as pulsed electric fields, UV light, cold atmospheric pressure plasma, and high- or low-energy electron beam.
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http://dx.doi.org/10.1146/annurev-food-032519-051632DOI Listing
March 2020

Biowaste treatment with black soldier fly larvae: Increasing performance through the formulation of biowastes based on protein and carbohydrates.

Waste Manag 2020 Feb 25;102:319-329. Epub 2019 Nov 25.

ETH Zurich: Swiss Federal Institute of Technology Zurich, Institute of Food, Nutrition and Health, Laboratory of Sustainable Food Processing, Schmelzbergstrasse 9, 8092 Zurich, Switzerland. Electronic address:

A key challenge for black soldier fly larvae (BSFL) treatment is its variable reliability and efficiency when applied to different biowastes. Similar to other biowaste treatment technologies, co-conversion could compensate for variability in the composition of biowastes. Using detailed nutrient analyses, this study assessed whether mixing biowastes to similar protein and non-fibre carbohydrate (NFC) contents increased the performance and reduced the variability of BSFL treatment in comparison to the treatment of individual wastes. The biowastes examined were mill by-products, human faeces, poultry slaughterhouse waste, cow manure, and canteen waste. Biowaste formulations had a protein-to-NFC ratio of 1:1, a protein content of 14-19%, and a NFC content of 13-15% (dry mass). Performance parameters that were assessed included survival and bioconversion rate, waste reduction, and waste conversion and protein conversion efficiency. In comparison to poultry feed (benchmark), vegetable canteen waste showed the best performance and cow manure performed worst. Formulations showed significantly improved performance and lower variability in comparison to the individual wastes. However, variability in performance was higher than expected for the formulations. One reason for this variability could be different fibre and lipid contents, which correlated with the performance results of the formulations. Overall, this research provides baseline knowledge and guidance on how BSFL treatment facilities may systematically operate using biowastes of varying types and compositions.
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http://dx.doi.org/10.1016/j.wasman.2019.10.036DOI Listing
February 2020

Perspective on Pulsed Electric Field Treatment in the Bio-based Industry.

Front Bioeng Biotechnol 2019 16;7:265. Epub 2019 Oct 16.

Laboratory of Sustainable Food Processing, Department of Health Sciences and Technology, Institute of Food Nutrition and Health, IFNH, ETH Zurich, Zurich, Switzerland.

The bio-based industry is urged to find solutions to meet the demands of a growing world population. In this context, increased resource efficiency is a major goal. Pulsed electric field (PEF) processing is a promising technological solution. Conventional PEF and the emerging area of nanosecond PEF (nsPEF) have been shown to induce various biological effects, with nsPEF inducing pronounced intracellular effects, which could provide solutions for currently faced challenges. Based on the flexibility and continuous operation of PEF and nsPEF processing, the technology can be integrated into many existing cultivation systems; its modularity provides an approach for inducing specific effects. Depending on the treatment conditions, selective inactivation, continuous extraction without impeding cell viability, as well as the stimulation of cell growth and/or cellular compound stimulation are potential applications in the bio-based industry. However, continuous treatment currently involves heterogeneous energy inputs. Increasing the homogeneity of PEF and nsPEF processing by considering the flow and electric field heterogeneity may allow for more targeted effects on biological cells, further increasing the potential of the technology for bio-based applications. We provide an overview of existing and potential applications of PEF and nsPEF and suggest that theoretical and practical analyses of flow and electric field heterogeneity may provide a basis for obtaining more targeted effects on biological cells and for further increasing the bio-based applications of the technology, which thereby could become a key technology for circular economy approaches in the future.
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http://dx.doi.org/10.3389/fbioe.2019.00265DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6805697PMC
October 2019

Continuous nanosecond pulsed electric field treatments foster the upstream performance of Chlorella vulgaris-based biorefinery concepts.

Bioresour Technol 2019 Dec 19;293:122029. Epub 2019 Aug 19.

ETH Zurich, Department of Health Sciences and Technology, Institute of Food, Nutrition and Health, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, Zurich 8092, Switzerland. Electronic address:

Nanosecond pulsed electric field treatment (nsPEF) is an innovative, technology-driven, and resource-efficient approach to foster the upstream performance of microalgae-based biorefinery concepts to transform microalgae into economic more viable raw materials for the biobased industry. A processing window applying three treatments of 100 ns, 5 Hz, and 10 kV cm to industrially relevant phototrophic Chlorella vulgaris in the early exponential growth phase significantly increased biomass yields by up to 17.53 ± 10.46% (p = 3.18 × 10). Treatments had limited effects on the carbon and pigment contents, but the protein content was decreased. The longest possible pulse width (100 ns) resulted in the highest biomass yield indicating underlying working mechanisms of enhanced cell proliferation based on intracellular and plasma membrane-related effects. The applicability to eukaryotes and prokaryotes, such as C. vulgaris and cyanobacteria highlights the possible impacts of nsPEF across multiple domains of the biobased industry relying on single-cell-based value-chains.
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http://dx.doi.org/10.1016/j.biortech.2019.122029DOI Listing
December 2019

Pulsed electric field based cyclic protein extraction of microalgae towards closed-loop biorefinery concepts.

Bioresour Technol 2019 Nov 24;291:121870. Epub 2019 Jul 24.

ETH Zurich, Department of Health Sciences and Technology, Institute of Food Nutrition and Health, IFNH, Laboratory of Sustainable Food Processing, Schmelzbergstrasse 9, Zurich 8092, Switzerland. Electronic address:

Microalgae-based biorefinery concepts can contribute to providing sufficient resources for a growing world population. However, the performance needs to be improved, which requires innovative technologies and processes. Continuous extraction from Chlorella vulgaris cultures via pulsed electric field (PEF) processing might be a viable process to increase the performance of microalgae-based biorefinery concepts. In this study, increasing protein extraction rates were observed with increasing electric field strength, up to 96.6 ± 4.8% of the free protein in the microalgae. However, increased extraction rates negatively influenced microalgae growth after PEF treatment. A free protein extraction rate up to 29.1 ± 1.1% without a significant influence on microalgal growth after 168 h was achieved (p = 0.788). Within the scope of this work, a protocol for continuous protein extraction during microalgae cultivation by PEF processing was developed. The incorporation of innovative downstream into upstream processing could be a viable future concept.
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http://dx.doi.org/10.1016/j.biortech.2019.121870DOI Listing
November 2019

Editorial: Microbial Decontamination by Novel Technologies - Mechanisms and Application Concepts.

Front Microbiol 2019 28;10:1476. Epub 2019 Jun 28.

Department of Food Science and Technology, Institute of Food Technology, University of Natural Resources and Life Sciences, Vienna, Austria.

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http://dx.doi.org/10.3389/fmicb.2019.01476DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6611343PMC
June 2019

Cultivation of Chlorella protothecoides under different growth modes and its utilisation in oil/water emulsions.

Bioresour Technol 2019 Sep 15;288:121476. Epub 2019 May 15.

ETH Zurich, Institute of Food, Nutrition and Health, Laboratory of Sustainable Food Processing, Schmelzbergstrasse 9, 8092 Zurich, Switzerland. Electronic address:

Microalgae can be incorporated in different bio-based products; however, the green colour is a barrier for a successful integration. This study aims to overcome this barrier by growing microalgae in different cultivation modes. Mixotrophic cultivation of Chlorella protothecoides resulted in the highest biomass production after 5 days (5.56 ± 0.09 g/L), followed by heterotrophic and photoautotrophic cultivation (4.33 ± 0.15 and 1.80 ± 0.05 g/L, respectively). Mixotrophically and heterotrophically produced biomass presented a reduced greenish colouration compared to photoautotrophically produced biomass. Chlorophyll content resulted in 1.46 ± 0.21 and 0.95 ± 0.28 mg/g dry weight (DW) in mixotrophic and heterotrophic cultures, respectively, and 25.98 ± 1.28 mg/g DW in photoautotrophic cultures. In contrast, the fraction of carotenoids in the total pigments was much higher. With the whole microalgae fractions after cell disruption as ingredients, stable emulsions containing 50% oil could be produced. No syneresis with serum separation was observed 24 h after preparation.
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http://dx.doi.org/10.1016/j.biortech.2019.121476DOI Listing
September 2019

Dietary Change Scenarios and Implications for Environmental, Nutrition, Human Health and Economic Dimensions of Food Sustainability.

Nutrients 2019 Apr 16;11(4). Epub 2019 Apr 16.

Laboratory of Sustainable Food Processing, ETH Zurich, Schmelzbergstrasse 9, 8092 Zurich, Switzerland.

Demand side interventions, such as dietary change, can significantly contribute towards the achievement of 2030 national sustainable development goals. However, most previous studies analysing the consequences of dietary change focus on a single dimension of sustainability (e.g., environment) using a limited number of indicators and dietary scenarios. A multi-dimension and multi-indicator analysis can identify the potential trade-offs. Here, starting from the current food consumption data (year 2011), we first designed nine alternative dietary scenarios (healthy Swiss diet, healthy global diet, vegetarian, vegan, pescatarian, flexitarian, protein-oriented and meat-oriented diets and a food greenhouse gas tax diet). Next we calculated three nutritional quality (nutrient balance score, disqualifying nutrient score, percent population with adequate nutrition), five environmental (greenhouse gas, water, land, nitrogen and phosphorus use), one economic (daily food expenditure) and one human health indicator (DALYs) for current and alternative diets. We found that transition towards a healthy diet following the guidelines of Swiss society of nutrition is the most sustainable option and is projected to result in 36% lesser environmental footprint, 33% lesser expenditure and 2.67% lower adverse health outcome (DALYs) compared with the current diet. On the other extreme, transition towards a meat or protein oriented diet can lead to large increases in diet related adverse health outcomes, environmental footprint, daily food expenditure and a reduction in intakes of essential nutrients (for Vitamin C, Fibre, Potassium and Calcium). We found that shifting to the vegetarian and vegan diet scenarios might lead to a reduction in intakes of certain micronutrients currently supplied primarily by animal-sourced foods (Vitamin B, Choline and Calcium). Results show that achieving a sustainable diet would entail a high reduction in the intake of meat and vegetable oils and a moderate reduction in cereals, roots and fish products and at the same time increased intake of legumes, nuts, seeds, fruits and vegetables. We identify several current data and research gaps that need to be filled in order to get more accurate results. Overall, our analysis underscores the need to consider multiple indicators while assessing the dietary sustainability and provides a template to conduct such studies in other countries and settings. Future efforts should focus on assessing the potential of different interventions and policies that can help transition the population from current to sustainable dietary patterns.
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http://dx.doi.org/10.3390/nu11040856DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6520741PMC
April 2019

Influence of Lactobacillus buchneri on soybean curd residue co-conversion by black soldier fly larvae (Hermetia illucens) for food and feedstock production.

Waste Manag 2019 Mar 1;86:114-122. Epub 2019 Feb 1.

State Key Laboratory of Agricultural Microbiology, National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China. Electronic address:

Black soldier fly larvae (BSFL), Hermetia illucens (Diptera: Stratiomyidae) can reduce environmental pollution and convert organic wastes into biomass that is rich in protein and fat. The influence of the nutritional characteristics of organic waste on BSFL characteristics relevant for food and feed safety remains poorly understood. To evaluate the conversion of soybean curd residues (SCR) into high-quality animal-derived proteins and fats for human and livestock consumption, this study assessed the co-conversion efficacy, nutrient composition, safety, and anti-nutritional factor concentrations in BSFL after the development on SCR with Lactobacillus buchneri (L3-9). SCR was pretreated with L. buchneri (10 cfu/ml), and then BSFL was employed for conversion. BSFL fed with SCR and L. buchneri had a significantly higher dry mass reduction (55.7 ± 0.9%), bioconversion rate (6.9 ± 0.3%), crude protein content (55.3 ± 0.6%), and fat content (30.0 ± 0.6%) than SCR (49.0 ± 0.7%, 5.0 ± 0.3%, 52.8 ± 0.3%, and 26.1 ± 0.8%, respectively) and artificial feed (43.9 ± 0.8%, 3.9 ± 0.1%, 50.3 ± 0.4%, and 24.3 ± 0.4%, respectively). However, the feed conversion ratio (8.0 ± 0.3), of BSFL fed with SCR and L. buchneri was lower than that of the BSFL fed with SCR (9.8 ± 0.1) and artificial feed (11.1 ± 0.5). In addition, BSFL had satisfactory concentrations of all essential amino acids and fatty acids required for human consumption as recommended by WHO/FAO/UNU. The heavy metals and anti-nutritional factor concentrations were within the safety intake levels for food and feedstock. Therefore, the addition of L. buchneri with BSFL on SCR did not only increase co-conversion performance but also enhanced the nutritional value of BSFL.
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http://dx.doi.org/10.1016/j.wasman.2019.01.022DOI Listing
March 2019

Superdormant Spores as a Hurdle for Gentle Germination-Inactivation Based Spore Control Strategies.

Front Microbiol 2018 4;9:3163. Epub 2019 Jan 4.

Sustainable Food Processing Laboratory, Institute of Food, Nutrition and Health, Department of Health Science and Technology, ETH Zurich, Zurich, Switzerland.

Bacterial spore control strategies based on the germination-inactivation principle can lower the thermal load needed to inactivate bacterial spores and thus preserve food quality better. However, the success of this strategy highly depends on the germination of spores, and a subpopulation of spores that fail to germinate or germinate extremely slowly hinders the application of this strategy. This subpopulation of spores is termed 'superdormant (SD) spores.' Depending on the source of the germination stimulus, SD spores are categorized as nutrient-SD spores, Ca-dipicolinic acid SD spores, dodecylamine-SD spores, and high pressure SD spores. In recent decades, research has been done to isolate these different groups of SD spores and unravel the cause of their germination deficiency as well as their germination capacities. This review summarizes the challenges caused by SD spores, their isolation and characterization, the underlying mechanisms of their germination deficiency, and the future research directions needed to tackle this topic in further depth.
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http://dx.doi.org/10.3389/fmicb.2018.03163DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6328458PMC
January 2019

and Spore Inactivation by Low Energy Electron Beam Technology: Resistance and Influencing Factors.

Front Microbiol 2018 23;9:2720. Epub 2018 Nov 23.

Sustainable Food Processing Laboratory, Institute of Food, Nutrition and Health, Department of Health Science and Technology, ETH Zurich, Zurich, Switzerland.

Low energy electron beam (LEEB) treatment is an emerging non-thermal technology that performs surface decontamination with a minimal influence on food quality. Bacterial spore resistance toward LEEB treatment and its influencing factors were investigated in this study. Spores from and species were treated with a lab-scale LEEB at energy levels of 80 and 200 keV. The spore resistances were expressed as -values (the radiation dose required for one log reduction at a given energy level) calculated from the linear regression of log reduction against absorbed dose of the sample. The results revealed that the spore inactivation efficiency by LEEB is comparable to that of other ionizing radiations and that the inactivation curves are mostly log-linear at the investigated dose range (3.8 - 8.2 kGy at 80 keV; 6.0 - 9.8 kGy at 200 keV). The -values obtained from the wildtype strains varied from 2.2 - 3.0 kGy at 80 keV, and from 2.2 - 3.1 kGy at 200 keV. mutant spores lacking α/β-type small, acid-soluble spore proteins showed decreased -values (1.3 kGy at 80 and 200 keV), indicating that spore DNA is one of the targets for LEEB spore inactivation. The results revealed that bacterial species, sporulation conditions and the treatment dose influence the spore LEEB inactivation. This finding indicates that for the application of this emerging technology, special attention should be paid to the choice of biological indicator, physiological state of the indicator and the processing settings. High spore inactivation efficiency supports the application of LEEB for the purpose of food surface decontamination. With its environmental, logistical, and economic advantages, LEEB can be a relevant technology for surface decontamination to deliver safe, minimally processed and additive-free food products.
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http://dx.doi.org/10.3389/fmicb.2018.02720DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6265500PMC
November 2018

Decomposition of biowaste macronutrients, microbes, and chemicals in black soldier fly larval treatment: A review.

Waste Manag 2018 Dec 8;82:302-318. Epub 2018 Nov 8.

ETH Zurich: Swiss Federal Institute of Technology Zurich, Institute of Food, Nutrition and Health, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, 8092 Zurich, Switzerland. Electronic address:

Processing of biowaste with larvae of the black soldier fly, Hermetia illucens L. (Diptera: Stratiomyidae), is an emerging waste treatment technology. Larvae grown on biowaste can be a relevant raw material for animal feed production and can therefore provide revenues for financially viable waste management systems. In addition, when produced on biowaste, insect-based feeds can be more sustainable than conventional feeds. Among others, the scalability of the technology will depend on the availability of large amounts of biowaste with a high process performance (e.g. bioconversion of organic matter to proteins and lipids) and microbial and chemical product safety. Currently, in contrast to other waste treatment technologies, such as composting or anaerobic digestion, the process performance is variable and the processes driving the decomposition of biowaste macronutrients, inactivation of microbes and fate of chemicals is poorly understood. This review presents the first summary of the most important processes involved in black soldier fly larvae (BSFL) treatment, based on the available knowledge concerning five well-studied fly species. This is a starting point to increase understanding regarding the processes of this technology, with the potential to increase its efficiency and uptake, and support the development of appropriate regulations. Based on this review, formulating different types of biowaste, e.g. to produce a diet with a similar protein content, a balanced amino acid profile and/or pre- and co-treatment of biowaste with beneficial microbes, has the potential to increase process performance. Following harvest, larvae require heat or other treatments for microbial inactivation and safety.
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http://dx.doi.org/10.1016/j.wasman.2018.10.022DOI Listing
December 2018

Effect of nanosecond pulsed electric field treatment on cell proliferation of microalgae.

Bioresour Technol 2019 Jan 26;271:402-408. Epub 2018 Sep 26.

ETH Zurich, Department of Health Sciences and Technology, Institute of Food, Nutrition and Health, IFNH, Sustainable Food Processing Laboratory, Schmelzbergstrasse 9, Zurich 8092, Switzerland. Electronic address:

Photoautotrophic microalgae based biorefinery concepts are currently not competitive compared to other established production systems. Therefore, innovative upstream processes need to be developed to increase the competitiveness of photoautotrophic microalgae biorefinery concepts. Abiotic sub-lethal stress induction via nanosecond pulsed electric field (nsPEF) treatment might be a viable process to increase the efficiency of photoautotrophic microalgae cultivation. In this work, an increased cell growth after nsPEF treatment was observable. Application of nsPEF to highly proliferating cells in a repetitive process resulted in a statistical significant increase in cell growth (p = 0.009). The effect was most pronounced after five days wherefore cellular structures and processes were analyzed to reveal a possible mechanism. Within this work, a protocol for increased cell proliferation with a possible mechanism was derived, which improves competitiveness of photoautotrophic microalgae biorefineries in the future. However, based on the derived mechanism, the results are also relevant for other microorganisms.
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http://dx.doi.org/10.1016/j.biortech.2018.09.124DOI Listing
January 2019

Trends in Microalgae Incorporation Into Innovative Food Products With Potential Health Benefits.

Front Nutr 2018 31;5:58. Epub 2018 Jul 31.

Laboratory of Sustainable Food Processing, Institute of Food Nutrition and Health IFNH, ETH Zurich, Zurich, Switzerland.

Microalgae have demonstrated potential to meet the population's need for a more sustainable food supply, specifically with respect to protein demand. These promising protein sources present several advantages over other currently used raw materials from an environmental point of view. Additionally, one of the main characteristics of microalgae is the production of bioactive compounds with potential benefits for human health. Microalgae exploitation as a source of protein (bulk protein) and other valuable products within the food industry still presents some drawbacks, mainly because of the underdeveloped technologies and processes currently available for microalgae processing. The systematic improvement of the technology readiness level (TRL) could help change the current situation if applied to microalgae cultivation and processing. High maturity in microalgae cultivation and processing technologies also requires improvement of the economy of scale and investment of resources in new facilities and research. Antioxidative, antihypertensive, immunomodulatory, anticancerogenic, hepato-protective, and anticoagulant activities have been attributed to some microalgae-derived compounds such as peptides. Nevertheless, research on this topic is scarce and the evidence on potential health benefits is not strong. In the last years, the possibility of using microalgae-derived compounds for innovative functional food products has become of great interest, but the literature available mainly focuses more on the addition of the whole cells or some compound already available on the market. This review describes the status of utilising microalgae as an ingredient in innovative food products with potential health benefits.
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http://dx.doi.org/10.3389/fnut.2018.00058DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080594PMC
July 2018

Comprehensive pulsed electric field (PEF) system analysis for microalgae processing.

Bioresour Technol 2018 Oct 7;265:268-274. Epub 2018 Jun 7.

ETH Zurich, Institute of Food Nutrition and Health, Laboratory of Sustainable Food Processing, Schmelzbergstrasse 9, Zurich 8092, Switzerland. Electronic address:

Pulsed electric field (PEF) is an emerging nonthermal technique with promising applications in microalgae biorefinery concepts. In this work, the flow field in continuous PEF processing and its influencing factors were analyzed and energy input distributions in PEF treatment chambers were investigated. The results were obtained using an interdisciplinary approach that combined multiphysics simulations with ultrasonic Doppler velocity profiling (UVP) and rheological measurements of Arthrospira platensis suspensions as a case study for applications in the biobased industry. UVP enabled non-invasive validation of multiphysics simulations. A. platensis suspensions follow a non-Newtonian, shear-thinning behavior, and measurement data could be fitted with rheological functions, which were used as an input for fluid dynamics simulations. Within the present work, a comprehensive system characterization was achieved that will facilitate research in the field of PEF processing.
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http://dx.doi.org/10.1016/j.biortech.2018.06.010DOI Listing
October 2018