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Biomolecules
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Invertebrates as Emerging Model Organisms in Nutrition Research
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Invertebrates as Emerging Model Organisms in Nutrition Research

A special issue of Biomolecules (ISSN 2218-273X). This special issue belongs to the section "Cellular Biochemistry".

Deadline for manuscript submissions: closed (15 February 2023) | Viewed by 46002

Special Issue Editor

Prof. Dr. Anika Wagner

E-Mail Website
Guest Editor
Institute of Nutritional Sciences, Justus-Liebig-University Giessen, Wilhelmstrasse 20, D-35392 Giessen, Germany
Interests: plant bioactives; host–diet interactions; inflammation; epigenetics; xenobiotic metabolism; stress response; energy metabolism; microbiota; aging

Special Issue Information

Dear Colleagues,

Animal models have been regularly used in basic research over the past few decades. With regard to nutritional sciences, initial results mainly derive from laboratory rodents, including rats and mice, as well as rabbits. The animal numbers in experimental settings with mice, in particular, have highly increased due to the possibility to specifically modify their genetic information. While mandatory protocols for animal handling with regard to minimizing pain, distress and killing have to be strictly followed, ethical concerns are still raised. Invertebrate models, including the fruit fly Drosophila melanogaster and the worm Caenorhabditis elegans, have been extensively used in basic biological research for decades. Although not mammalians, these model organisms increasingly find their way into the investigation of scientific questions with more physiological approaches. As most essential signaling pathways are evolutionarily conserved in invertebrates, they are progressively used to answer essential research questions within nutritional sciences. Invertebrate models offer the possibility to investigate effects of, e.g., dietary regimens and/or specific nutrients on aging, infection, inflammation, epigenetics, chemoprevention, etc., in a higher number of animals, within a shorter period of time and with lower costs and ethical concerns.

The present Special Issue aims to provide an overview of invertebrate model organisms with their advantages and disadvantages that qualify them to be used in nutrition research. We also encourage contributions addressing the effects of nutritional factors on immune function, chemoprevention and epigenetic mechanisms in invertebrate model organisms. Both original articles, as well as review articles, are welcome to this Special Issue.

Prof. Dr. Anika Wagner
Guest Editor

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Keywords

  • invertebrates (Drosophila melanogaster, Caenorhabditis elegans, etc.)
  • nutrition/diet (dietary regimens, bioactive compounds, etc.)
  • chemoprevention
  • immune function
  • epigenetic mechanisms

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Published Papers (9 papers)

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Research

Jump to: Review

25 pages, 2883 KiB  
Article
Temperature- and Diet-Induced Plasticity of Growth and Digestive Enzymes Activity in Spongy Moth Larvae
by Jelica Lazarević, Slobodan Milanović, Darka Šešlija Jovanović and Milena Janković-Tomanić
Biomolecules 2023, 13(5), 821; https://doi.org/10.3390/biom13050821 - 11 May 2023
Cited by 3 | Viewed by 2365
Abstract
Temperature and food quality are the most important environmental factors determining the performance of herbivorous insects. The objective of our study was to evaluate the responses of the spongy moth (formerly known as the gypsy moth) [Lymantria dispar L. (Lepidoptera: Erebidae)] to [...] Read more.
Temperature and food quality are the most important environmental factors determining the performance of herbivorous insects. The objective of our study was to evaluate the responses of the spongy moth (formerly known as the gypsy moth) [Lymantria dispar L. (Lepidoptera: Erebidae)] to simultaneous variation in these two factors. From hatching to the fourth instar, larvae were exposed to three temperatures (19 °C, 23 °C, and 28 °C) and fed four artificial diets that differed in protein (P) and carbohydrate (C) content. Within each temperature regime, the effects of the nutrient content (P+C) and ratio (P:C) on development duration, larval mass, growth rate, and activities of digestive proteases, carbohydrases, and lipase were examined. It was found that temperature and food quality had a significant effect on the fitness-related traits and digestive physiology of the larvae. The greatest mass and highest growth rate were obtained at 28 °C on a high-protein low-carbohydrate diet. A homeostatic increase in activity was observed for total protease, trypsin, and amylase in response to low substrate levels in the diet. A significant modulation of overall enzyme activities in response to 28 °C was detected only with a low diet quality. A decrease in the nutrient content and P:C ratio only affected the coordination of enzyme activities at 28 °C, as indicated by the significantly altered correlation matrices. Multiple linear regression analysis showed that variation in fitness traits in response to different rearing conditions could be explained by variation in digestion. Our results contribute to the understanding of the role of digestive enzymes in post-ingestive nutrient balancing. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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9 pages, 1366 KiB  
Article
Dietary Choice Reshapes Metabolism in Drosophila by Affecting Consumption of Macronutrients
by Olha Strilbytska, Uliana Semaniuk, Volodymyr Bubalo, Kenneth B. Storey and Oleh Lushchak
Biomolecules 2022, 12(9), 1201; https://doi.org/10.3390/biom12091201 - 30 Aug 2022
Cited by 6 | Viewed by 2052
Abstract
The precise regulation of metabolism and feeding behavior is important for preventing the development of metabolic diseases. Here we examine the effects on Drosophila metabolism of dietary choice. These changes are predicted to be dependent on both the quantity and quality of the [...] Read more.
The precise regulation of metabolism and feeding behavior is important for preventing the development of metabolic diseases. Here we examine the effects on Drosophila metabolism of dietary choice. These changes are predicted to be dependent on both the quantity and quality of the chosen diet. Using a geometric framework for both no-choice and two-choice conditions, we found that feeding decisions led to higher glucose and trehalose levels but lower triglycerides pools. The feeding regimens had similar strategies for macronutrient balancing, and both maximized hemolymph glucose and glycogen content under low protein intake. In addition, the flies showed significant differences in the way they regulated trehalose and triglyceride levels in response to carbohydrate and protein consumption between choice and no-choice nutrition. Under choice conditions, trehalose and triglyceride levels were maximized at the lowest protein and carbohydrate consumption. Thus, we suggest that these changes in carbohydrate and lipid metabolism are caused by differences in the macronutrients consumed by flies. Food choice elicits rapid metabolic changes to maintain energy homeostasis. These results contribute to our understanding of how metabolism is regulated by the revealed nutrient variation in response to food decisions. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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18 pages, 2544 KiB  
Article
Vitamin A Deficiency Alters the Phototransduction Machinery and Distinct Non-Vision-Specific Pathways in the Drosophila Eye Proteome
by Mukesh Kumar, Canan Has, Khanh Lam-Kamath, Sophie Ayciriex, Deepshe Dewett, Mhamed Bashir, Clara Poupault, Kai Schuhmann, Oskar Knittelfelder, Bharath Kumar Raghuraman, Robert Ahrends, Jens Rister and Andrej Shevchenko
Biomolecules 2022, 12(8), 1083; https://doi.org/10.3390/biom12081083 - 6 Aug 2022
Cited by 5 | Viewed by 4022
Abstract
The requirement of vitamin A for the synthesis of the visual chromophore and the light-sensing pigments has been studied in vertebrate and invertebrate model organisms. To identify the molecular mechanisms that orchestrate the ocular response to vitamin A deprivation, we took advantage of [...] Read more.
The requirement of vitamin A for the synthesis of the visual chromophore and the light-sensing pigments has been studied in vertebrate and invertebrate model organisms. To identify the molecular mechanisms that orchestrate the ocular response to vitamin A deprivation, we took advantage of the fact that Drosophila melanogaster predominantly requires vitamin A for vision, but not for development or survival. We analyzed the impacts of vitamin A deficiency on the morphology, the lipidome, and the proteome of the Drosophila eye. We found that chronic vitamin A deprivation damaged the light-sensing compartments and caused a dramatic loss of visual pigments, but also decreased the molar abundance of most phototransduction proteins that amplify and transduce the visual signal. Unexpectedly, vitamin A deficiency also decreased the abundances of specific subunits of mitochondrial TCA cycle and respiratory chain components but increased the levels of cuticle- and lens-related proteins. In contrast, we found no apparent effects of vitamin A deficiency on the ocular lipidome. In summary, chronic vitamin A deficiency decreases the levels of most components of the visual signaling pathway, but also affects molecular pathways that are not vision-specific and whose mechanistic connection to vitamin A remains to be elucidated. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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13 pages, 2087 KiB  
Article
Ingestion of Diazotrophs Makes Corals More Resistant to Heat Stress
by Valentine Meunier, Sophie Bonnet, Mercedes Camps, Mar Benavides, Jeff Dubosc, Riccardo Rodolfo-Metalpa and Fanny Houlbrèque
Biomolecules 2022, 12(4), 537; https://doi.org/10.3390/biom12040537 - 2 Apr 2022
Cited by 3 | Viewed by 3387
Abstract
Over the past decade, coral bleaching events have continued to recur and intensify. During bleaching, corals expel millions of their symbionts, depriving the host from its main food source. One mechanism used by corals to resist bleaching consists in exploiting food sources other [...] Read more.
Over the past decade, coral bleaching events have continued to recur and intensify. During bleaching, corals expel millions of their symbionts, depriving the host from its main food source. One mechanism used by corals to resist bleaching consists in exploiting food sources other than autotrophy. Among the food sources available in the reefs, dinitrogen (N2)-fixing prokaryotes or planktonic diazotrophs (hereafter called ‘PD’) have the particularity to reduce atmospheric dinitrogen (N2) and release part of this nitrogen (diazotroph-derived nitrogen or DDN) in bioavailable form. Here, we submitted coral colonies of Stylophora pistillata, fed or not with planktonic diazotrophs, to a temperature stress of up to 31 ± 0.5 °C and measured their physiological responses (photosynthetic efficiency, symbiont density, and growth rates). Heat-unfed colonies died 8 days after the heat stress while heat-PD-fed corals remained alive after 10 days of heat stress. The supply of PD allowed corals to maintain minimal chlorophyll concentration and symbiont density, sustaining photosynthetic efficiency and stimulating coral growth of up to 48% compared to unfed ones. By providing an alternative source of bioavailable nitrogen and carbon, this specific planktonic diazotroph feeding may have a profound potential for coral bleaching recovery. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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13 pages, 2217 KiB  
Article
Drosophila melanogaster as a Model Organism for Obesity and Type-2 Diabetes Mellitus by Applying High-Sugar and High-Fat Diets
by Nieves Baenas and Anika E. Wagner
Biomolecules 2022, 12(2), 307; https://doi.org/10.3390/biom12020307 - 14 Feb 2022
Cited by 20 | Viewed by 6925
Abstract
Several studies have been published introducing Drosophila melanogaster as a research model to investigate the effects of high-calorie diets on metabolic dysfunctions. However, differences between the use of high-sugar diets (HSD) and high-fat diets (HFD) to affect fly physiology, as well as the [...] Read more.
Several studies have been published introducing Drosophila melanogaster as a research model to investigate the effects of high-calorie diets on metabolic dysfunctions. However, differences between the use of high-sugar diets (HSD) and high-fat diets (HFD) to affect fly physiology, as well as the influence on sex and age, have been seldom described. Thus, the aim of the present work was to investigate and compare the effects of HSD (30% sucrose) and HFD (15% coconut oil) on symptoms of metabolic dysfunction related to obesity and type-2 diabetes mellitus, including weight gain, survival, climbing ability, glucose and triglycerides accumulation and expression levels of Drosophila insulin-like peptides (dIlps). Female and male flies were subjected to HSD and HFD for 10, 20 and 30 days. The obtained results showed clear differences in the effects of both diets on survival, glucose and triglyceride accumulation and dIlps expression, being gender and age determinant. The present study also suggested that weight gain does not seem to be an appropriate parameter to define fly obesity, since other characteristics appear to be more meaningful in the development of obesity phenotypes. Taken together, the results demonstrate a key role for both diets, HSD and HFD, to induce an obese fly phenotype with associated diseases. However, further studies are needed to elucidate the underlying molecular mechanisms how both diets differently affect fly metabolism. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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19 pages, 1957 KiB  
Article
Sexual Dimorphism in Metabolic Responses to Western Diet in Drosophila melanogaster
by Sofie De Groef, Tom Wilms, Séverine Balmand, Federica Calevro and Patrick Callaerts
Biomolecules 2022, 12(1), 33; https://doi.org/10.3390/biom12010033 - 27 Dec 2021
Cited by 10 | Viewed by 3769
Abstract
Obesity is a chronic disease affecting millions of people worldwide. The fruit fly (Drosophila melanogaster) is an interesting research model to study metabolic and transcriptomic responses to obesogenic diets. However, the sex-specific differences in these responses are still understudied and perhaps [...] Read more.
Obesity is a chronic disease affecting millions of people worldwide. The fruit fly (Drosophila melanogaster) is an interesting research model to study metabolic and transcriptomic responses to obesogenic diets. However, the sex-specific differences in these responses are still understudied and perhaps underestimated. In this study, we exposed adult male and female Dahomey fruit flies to a standard diet supplemented with sugar, fat, or a combination of both. The exposure to a diet supplemented with 10% sugar and 10% fat efficiently induced an increase in the lipid content in flies, a hallmark for obesity. This increase in lipid content was more prominent in males, while females displayed significant changes in glycogen content. A strong effect of the diets on the ovarian size and number of ma-ture oocytes was also present in females exposed to diets supplemented with fat and a combina-tion of fat and sugar. In both males and females, fat body morphology changed and was associ-ated with an increase in lipid content of fat cells in response to the diets. The expression of me-tabolism-related genes also displayed a strong sexually dimorphic response under normal condi-tions and in response to sugar and/or fat-supplemented diets. Here, we show that the exposure of adult fruit flies to an obesogenic diet containing both sugar and fat allowed studying sexual dimorphism in metabolism and the expression of genes regulating metabolism. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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Review

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20 pages, 1538 KiB  
Review
Insect Models in Nutrition Research
by Miray Tonk-Rügen, Andreas Vilcinskas and Anika E. Wagner
Biomolecules 2022, 12(11), 1668; https://doi.org/10.3390/biom12111668 - 11 Nov 2022
Cited by 7 | Viewed by 4501
Abstract
Insects are the most diverse organisms on earth, accounting for ~80% of all animals. They are valuable as model organisms, particularly in the context of genetics, development, behavior, neurobiology and evolutionary biology. Compared to other laboratory animals, insects are advantageous because they are [...] Read more.
Insects are the most diverse organisms on earth, accounting for ~80% of all animals. They are valuable as model organisms, particularly in the context of genetics, development, behavior, neurobiology and evolutionary biology. Compared to other laboratory animals, insects are advantageous because they are inexpensive to house and breed in large numbers, making them suitable for high-throughput testing. They also have a short life cycle, facilitating the analysis of generational effects, and they fulfil the 3R principle (replacement, reduction and refinement). Many insect genomes have now been sequenced, highlighting their genetic and physiological similarities with humans. These factors also make insects favorable as whole-animal high-throughput models in nutritional research. In this review, we discuss the impact of insect models in nutritional science, focusing on studies investigating the role of nutrition in metabolic diseases and aging/longevity. We also consider food toxicology and the use of insects to study the gut microbiome. The benefits of insects as models to study the relationship between nutrition and biological markers of fitness and longevity can be exploited to improve human health. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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19 pages, 761 KiB  
Review
Caenorhabditis elegans as a Model for the Effects of Phytochemicals on Mitochondria and Aging
by Fabian Schmitt and Gunter P. Eckert
Biomolecules 2022, 12(11), 1550; https://doi.org/10.3390/biom12111550 - 24 Oct 2022
Cited by 4 | Viewed by 3980
Abstract
The study of aging is an important topic in contemporary research. Considering the demographic changes and the resulting shifts towards an older population, it is of great interest to preserve youthful physiology in old age. For this endeavor, it is necessary to choose [...] Read more.
The study of aging is an important topic in contemporary research. Considering the demographic changes and the resulting shifts towards an older population, it is of great interest to preserve youthful physiology in old age. For this endeavor, it is necessary to choose an appropriate model. One such model is the nematode Caenorhabditis elegans (C. elegans), which has a long tradition in aging research. In this review article, we explore the advantages of using the nematode model in aging research, focusing on bioenergetics and the study of secondary plant metabolites that have interesting implications during this process. In the first section, we review the situation of aging research today. Conventional theories and hypotheses about the ongoing aging process will be presented and briefly explained. The second section focuses on the nematode C. elegans and its utility in aging and nutrition research. Two useful genome editing methods for monitoring genetic interactions (RNAi and CRISPR/Cas9) are presented. Due to the mitochondria’s influence on aging, we also introduce the possibility of observing bioenergetics and respiratory phenomena in C. elegans. We then report on mitochondrial conservation between vertebrates and invertebrates. Here, we explain why the nematode is a suitable model for the study of mitochondrial aging. In the fourth section, we focus on phytochemicals and their applications in contemporary nutritional science, with an emphasis on aging research. As an emerging field of science, we conclude this review in the fifth section with several studies focusing on mitochondrial research and the effects of phytochemicals such as polyphenols. In summary, the nematode C. elegans is a suitable model for aging research that incorporates the mitochondrial theory of aging. Its living conditions in the laboratory are optimal for feeding studies, thus enabling bioenergetics to be observed during the aging process. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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83 pages, 8081 KiB  
Review
Phenotyping of Drosophila Melanogaster—A Nutritional Perspective
by Virginia Eickelberg, Kai Lüersen, Stefanie Staats and Gerald Rimbach
Biomolecules 2022, 12(2), 221; https://doi.org/10.3390/biom12020221 - 27 Jan 2022
Cited by 14 | Viewed by 13375
Abstract
The model organism Drosophila melanogaster was increasingly applied in nutrition research in recent years. A range of methods are available for the phenotyping of D. melanogaster, which are outlined in the first part of this review. The methods include determinations of body [...] Read more.
The model organism Drosophila melanogaster was increasingly applied in nutrition research in recent years. A range of methods are available for the phenotyping of D. melanogaster, which are outlined in the first part of this review. The methods include determinations of body weight, body composition, food intake, lifespan, locomotor activity, reproductive capacity and stress tolerance. In the second part, the practical application of the phenotyping of flies is demonstrated via a discussion of obese phenotypes in response to high-sugar diet (HSD) and high-fat diet (HFD) feeding. HSD feeding and HFD feeding are dietary interventions that lead to an increase in fat storage and affect carbohydrate-insulin homeostasis, lifespan, locomotor activity, reproductive capacity and stress tolerance. Furthermore, studies regarding the impacts of HSD and HFD on the transcriptome and metabolome of D. melanogaster are important for relating phenotypic changes to underlying molecular mechanisms. Overall, D. melanogaster was demonstrated to be a valuable model organism with which to examine the pathogeneses and underlying molecular mechanisms of common chronic metabolic diseases in a nutritional context. Full article
(This article belongs to the Special Issue Invertebrates as Emerging Model Organisms in Nutrition Research)
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