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Goyache, I.; Yavorov-Dayliev, D.; Milagro, F.I.; Aranaz, P. Caenorhabditis elegans for Screening Probiotics with Antiobesity Properties. Encyclopedia. Available online: https://encyclopedia.pub/entry/54866 (accessed on 28 April 2024).
Goyache I, Yavorov-Dayliev D, Milagro FI, Aranaz P. Caenorhabditis elegans for Screening Probiotics with Antiobesity Properties. Encyclopedia. Available at: https://encyclopedia.pub/entry/54866. Accessed April 28, 2024.
Goyache, Ignacio, Deyan Yavorov-Dayliev, Fermín I. Milagro, Paula Aranaz. "Caenorhabditis elegans for Screening Probiotics with Antiobesity Properties" Encyclopedia, https://encyclopedia.pub/entry/54866 (accessed April 28, 2024).
Goyache, I., Yavorov-Dayliev, D., Milagro, F.I., & Aranaz, P. (2024, February 07). Caenorhabditis elegans for Screening Probiotics with Antiobesity Properties. In Encyclopedia. https://encyclopedia.pub/entry/54866
Goyache, Ignacio, et al. "Caenorhabditis elegans for Screening Probiotics with Antiobesity Properties." Encyclopedia. Web. 07 February, 2024.
Caenorhabditis elegans for Screening Probiotics with Antiobesity Properties
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This entry is adapted from the peer-reviewed paper 10.3390/ijms25021321

Due to the role of gut microbiota in the regulation of lipid, glucose, and insulin homeostasis, probiotics with beneficial properties have emerged as an alternative therapeutic tool to ameliorate metabolic diseases-related disturbances, including fat excess or inflammation. Different strains of bacteria, mainly lactic acid bacteria (LAB) and species from the genus Bifidobacterium, have emerged as potential probiotics due to their anti-obesogenic and/or anti-diabetic properties. However, in vivo studies are needed to demonstrate the mechanisms involved in these probiotic features. In this context, Caenorhabditis elegans has emerged as a very powerful simple in vivo model to study the physiological and molecular effects of probiotics with potential applications regarding the different pathologies of metabolic syndrome.

gut microbiota probiotics obesity diabetes bacteria postbiotics

1. Introduction

During the last few years, different research studies have evidenced the important role that the gut microbiota plays in the metabolic health of the host [1][2]. In this context, different research groups have identified specific modifications in the gut bacterial composition that could be associated with a differential risk of developing metabolic syndrome diseases, including obesity or diabetes, and which seem to play a fundamental role in the appearance of metabolic complications associated with these diseases, such as the increase in oxidative stress and chronic low-grade inflammation [3][4][5][6][7][8][9]. For this reason, it is not surprising that the modulation of the intestinal microbiota towards a healthier bacterial composition is currently considered a major factor to bear in mind for the development of therapeutic strategies in the treatment or prevention of metabolic diseases [10][11][12].
One of the best-known strategies for modulating gut microbiota is the use of probiotics. Probiotics are defined by the Food and Agriculture Organization (FAO) and the World Health Organization (WHO) as “live microorganisms which when administered in adequate amounts confer a health benefit on the host” [13]. Thus, different bacterial strains, mainly lactic acid bacteria (LAB) and strains from the genus Bifidobacterium, have emerged as potential treatments due to their health-promoting properties, including lipid-reducing activities, or the maintenance of glucose homeostasis, among others [14][15][16][17]. However, the mechanisms of action of some of these probiotic strains are scarcely understood. For this reason, in vivo studies are necessary to understand the molecular mechanisms involved in the metabolic effects observed with the incorporation of these probiotics into the diet. In this sense, the use of simple in vivo models such as Caenorhabditis elegans (C. elegans) represents a quick and effective advantage to describe these beneficial activities and understand the molecular mechanisms involved [18].
C. elegans has been widely employed as an animal model in different diseases and physiological processes, including obesity, diabetes, aging, and neurodegenerative disorders [19][20][21]. This microscopic nematode can be cultured and manipulated at low cost through conventional in vitro methods, which confers a great advantage as an in vivo model, in addition to its transparency, large number of progenies, short life span, and completely sequenced genomes [20][21]. Interestingly, the high conservation in humans of the genes involved in lipid and carbohydrate regulation makes C. elegans an excellent model for exploring energy homeostasis and the regulation of cellular lipid storage [22]. Thus, despite its simplicity, this nematode is currently considered a powerful experimental model for the study of physiological and molecular effects of health-promoting compounds, including probiotics, with potential applications in the different pathologies of metabolic syndrome [23][24].

2. Probiotics with Lipid-Reducing Activity in C. elegans

In the last decade, the use of simple in vivo models such as C. elegans has been demonstrated to represent a powerful method to investigate microorganism–host interactions, as well as to evaluate the antioxidant, anti-aging, and life-extending properties of different probiotics strains [25]. Different Bifidobacteria and Lactobacilli strains have been demonstrated to extend nematode lifespan, mainly through modulations in the p-38 mitogen-activated protein kinases (p38-MAPK) signaling pathway [26]. For example, a recent study demonstrated that supplementation with Bacillus subtilis DG101, isolated from the traditional Japanese fermented food Nattō, extended worm lifespan by 45% and improved chemotaxis, in comparison with E. coli OP50-fed worms [27]. Similarly, supplementation with Lacticaseibacillus casei 62 and Lacticaseibacillus casei 63 increased nematode lifespan by improving the mitochondrial function, suggesting these bacterial strains as potential probiotics in sarcopenia [28].
However, the information about the potential anti-lipogenic, anti-diabetic, or anti-inflammatory properties of certain probiotic strains has been scarcely described in C. elegans [29]. Researchers summarized all the research describing potential anti-obesity or anti-diabetic properties of potential probiotic bacterial strains in C. elegans. The fat-reducing activities, cholesterol modulation, and the ability to counteract the effect of high-glucose exposure were some of the properties described for these probiotics.
C. elegans stores fat in lipid droplets accumulated in intestinal and skin-like hypodermal cells, mainly in the form of triglycerides [22]. Thus, probiotics might modulate lipid accumulation in C. elegans by affecting different signaling pathways, such as suppressing glucose uptake or triglyceride synthesis or activating fatty acid β-oxidation [30]. The main bacterial strains with fat-reducing activities are summarized in Table 1.
Table 1. Summary of the studies using C. elegans to screen probiotic strains with anti-inflammatory properties.
Probiotic Strain Food Source and Culture Conditions Main Findings Mechanisms (Signaling Pathways Involved) Reference
Probiotic cocktail containing five Lactobacillus and five Enterococcus strains isolated from healthy infants E. coli OP50 with or without taurine;
Supplementation of synchronized worms from L1 stage;
(proof of concept of the probiotic bile hydrolase activity).		 ↓ leaky gut (smurf assay)
↑ motility
↑ worm survival		 Not described in C. elegans. [31]
Lactobacillus gasseri SBT2055 E. coli OP50 or Lactobacillus gasseri SBT2055 (live or UV killed);
20 °C;
L1 to L4/adult.		 ↑ worm survival
↓ aging (lipofuscin)
↑ Oxidative stress response (Paraquat asay)
↑ Mitochondrial function measured by MitoTracker® CMXRos and cyanine dye JC-1		 Skn-1, nsy-1, sek-1, and pmk-1 dependant mechanism for life-extension via p38 MAPK pathway signaling.
Independent effects from daf-2 or daf-16.
Upregulation of oxidative stress related genes: skn-1, gst-4, sod-1, trx-1 (thioredoxin), clk-1 (mitochondrial polypeptide), hsp16.2 (heat-shock protein), hsp-70, and gcs-1 (an ortholog of γ-glutamyl-cysteine synthetase).		 [32]
Propionibacterium freudenreichii KCTC 1063 E. coli OP50 or Propionibacterium freudenreichii KCTC 1063;
25 °C;
Assays performed on L4 adults.		 ↑ worm survival
↓ aging (lipofuscin)
resistance to Salmonella typhimurium		 Skn-1 mutants failed to benefit from extended life.
Upregulation of p38/MAPKK pathway genes daf-2, pmk-1, sek-1, mek-1, dbl-1, daf-7, sma-3, and daf-12.
Upregulation of antimicrobial peptide-related genes lys-7 and lys-8.		 [33]
Lactobacillus fermentum Strain JDFM216 E. coli OP50 or Lactobacillus fermentum JDFM216;
25 °C;
L1 to L4/adult.		 ↑ worm survival
↑ Resistance to food-borne pathogens, including Staphylococcus aureus and E. coli O157:H7		 Upregulation of the NHR and PMK-1 pathway. [34]
Bacillus amyloliquefaciens SCGB1 Exposure to E. coli O157:H7 or Bacillus amyloliquefaciens SCGB1. ↑ worm survival upon exposure to pathogen E. coli O157:H7. Upregulation of pmk-1. [35]
Lactococcus cremoris subsp. cremoris E. coli OP50 or Lactococcus cremoris subsp. Cremoris;
25 °C;
Young adult worms.		 ↑ Resistance to Salmonella enterica subsp. enterica serovar Enteritidis or Staphylococcus aureus
↓ aging (lipofuscin)		 No beneficial effects on skn-1 lacking mutants.
Upregulation of heme oxygenase-1 ho-1, effector of the SKN-1/Nrf2 pathway.		 [36]
↑: increased; ↓: reduced.

2.1. Bifidobacterium Strains with Anti-Obesity Properties in C. elegans

One of the first studies using C. elegans for the study of probiotic properties was published by Martorell et al. [23] (Table 1). In their work, this group performed a screening of the potential lipid-reducing activities of a Biopolis collection of 38 Lactobacillus (23) and Bifidobacterium (15) strains, previously isolated from the feces of healthy breast-fed babies. They found that the supplementation of the nematode growth medium (NGM) agar with a specific strain of Bifidobacterium animalis subsp. lactis CECT 8145 induced a reduction of approximately 33% in the lipid content of the worm, in comparison with nematodes fed E. coli OP50 as a standard diet. This reduction in fat accumulation was also maintained in soy-fermented milk treated with Bifidobacterium animalis subsp. lactis CECT 8145 [37]. Moreover, treatment with this Bifidobacterium strain also induced an improvement of the nematode oxidative stress-response, and an increase in lifespan by 64%. Gene expression analyses demonstrated the involvement of genes involved in energy metabolism, including the beta-oxidation genes acox-1 and daf-22, the energy modulator daf-16, and the unsaturated fatty acid synthesis gene fat-7, which was overexpressed in CECT 8145-treated worms (Figure 1).
Figure 1. Schematic representation of different signaling pathways affected by the probiotic strains with anti-obesity or anti-diabetic properties in C. elegans. The figure includes a representation of the IIS signaling pathway, fatty acid synthesis, fatty acid β-oxidation, and oxidative stress responses.
Interestingly, the use of an inactivated form of Bifidobacterium animalis subsp. lactis CECT 8145 (BPL1), obtained via heat treatment (70 °C for 18 h) induced a similar reduction in the nematode fat content to that of the active form, supporting the idea that the strain efficacy still remained stable in non-viable cells, and that cell wall components might be responsible for the anti-obesogenic properties of this strain [23]. In this context, a subsequent study by this group demonstrated that an infant milk formula supplemented with heat-treated Bifidobacterium animalis subsp. lactis CECT 8145 (HT-BPL1, as a postbiotic) significantly reduced the fat content in C. elegans, confirming the anti-obesogenic properties of this strain in the nematode [37]. Further investigations demonstrated that lipoteichoic acid (LTA), a postbiotic isolated from the BPL1, was responsible for its lipid-reducing activities, both in NGM plates and glucose-loaded conditions [38]. In their work, Balaguer et al. demonstrated that the anti-lipogenic activities of both BPL1 and LTA were independent of SKN-1/p-38 MAPK pathway but were mediated by the modulation of the insulin-like signaling pathway (IGF-1), due to the lack of fat-reducing activity in daf-2 and daf-16 mutants [38].

2.2. Pediococcus acidilactici Strains with Anti-Obesity Properties in C. elegans

One of the bacterial species that has emerged in recent years as a potential probiotic with anti-obesogenic and anti-diabetic properties is Pediococcus acidilactici [39][40][41][42][43]. Thus, different research groups have evaluated the potential beneficial activities of Pediococcus acidilactici strains on lipid and carbohydrate metabolism using C. elegans (Table 1) [39][44][45]. In their study, Daliri et al. isolated lactic acid bacteria (LAB) strains from Korean fermented soybean paste, which included Pediococcus acidilactici SDL1402 and P. acidilactici SDL1406, together with Weisella cibaria SCCB2306 and Lactobacillus rhamnosus JDFM6 strains [45]. These four strains were able to reduce cholesterol levels in C. elegans, and increase the lifespan of the worms in comparison to E. coli OP50-fed worms [45].
In a similar study performed by Barathikannan et al. [44], a novel strain of Pediococcus acidilactici MNL5 was isolated through the screening of thirty-two LABs from fermented Indian herbal medicine with health-promoting activities in C. elegans. P. acidilactici MNL5 was able to counteract the lifespan-reduction induced by glucose supplementation in the medium, together with a reduction in fat accumulation, in comparison with E. coli OP50-fed worms [44]. Gene expression analysis suggested that P. acidilactici MNL5 inhibited de novo lipogenesis by down-regulating the fatty acid desaturase-coding genes fat-4, fat-5, and fat-6, inducing a reduction in lipid accumulation (Figure 1) [44].
Similarly, the researchers' group demonstrated the anti-obesogenic and anti-diabetic properties of the strain Pediococcus acidilactici CECT 9879 (p1Ac®) in C. elegans [24][39] and rodents [39][43]. This strain was able to counteract the effect of glucose on C. elegans fat accumulation, lifespan, oxidative stress, and aging [24]. Thus, supplementation with P. acidilactici CECT 9879 at a dose of 5 × 106 CFU/mL (in combination with the nematode standard diet E. coli OP50) was able to significantly reduce the nematode fat content in comparison with nematodes grown with OP50 only. Moreover, the probiotic was able to counteract the effect of high-glucose conditions by ameliorating aging (reducing lipofuscin pigment), enhancing the stress–oxidative response and prolonging lifespan without affecting worm development [24].
Gene expression analysis and mutant assays demonstrated that P. acidilactici CECT 9879 exerted health-promoting activities by affecting the IIS signaling pathway, by increasing the expression of daf-16, but also affecting the SKN-1/Nrf-2 signaling pathway. Moreover, the anti-obesity and anti-diabetic properties of P. acidilactici CECT 9879 included the inhibition of fatty acid biosynthesis (via the downregulation of fasn-1, fat-5, fat-7, and mdt-15 genes), and inducing FA degradation (by increasing the expression β-oxidation genes acox-1, daf-22, maoc-1, and cpt-2) (Figure 1) [24]. The properties of this probiotic strain and the molecular mechanism of action were confirmed and maintained in a subsequent study where P. acidilactici CECT 9879 was combined with the prebiotic ingredients chromium picolinate (0.5 μg/mL) and oat-beta glucans (50 μg/mL) [39]. Taken together, the research performed in C. elegans demonstrates the potential anti-obesity and anti-diabetic properties of P. acidilactici strains and supports the need for additional studies in higher models to determine its possible application in humans.

2.3. Other Lactic Acid Bacteria with Anti-Obesity Properties in C. elegans

Lactic acid bacteria (LAB) are important compositors of gut microbiota due to their beneficial properties by inhibiting the growth of pathogenic bacteria, enhancing intestinal function, modulating metabolic functions, and regulating the immune system. Thus, like Pediococcus, other LAB have been described to exert fat-reducing activities in C. elegans. In their study, Marquez et al. [30] described the anti-obesity properties of a probiotic mixture Lactobacillus delbrueckii subsp. indicus CRL1447, to which a mix of probiotics consisting of Limosilactobacillus fermentum CRL1446, Lactiplantibacillus paraplantarum CRL1449, and CRL1472 strains was then added in different formulations (Table 1). This combination was able to reduce worm TG content, when combined with E. coli OP50 at a ratio 25:75, in comparison with 100% of E. coli OP50 [30].
An interesting study performed by Gu et al. [46] described the efficacy of a probiotic strain of Lactobacillus pentosus MJM60383 in an obese model of C. elegans (Table 1). In this work, they established a new obesity model by feeding this nematode with a culture of Enterobacter cloacae, a proposed pathogenic bacterium that induces obesity in germ-free mice, in combination with high-glucose (100 mM) conditions (HGD-E) [46]. The proposed C. elegans obese model was characterized by an increase in the lipogenic and a decrease in the β-oxidation genes. With this model, they demonstrated that supplementation with L. pentosus MJM60383 strain was able to significantly reduce C. elegans fat accumulation, counteracting the effect of the obesity-related pathogenic bacteria E. cloacae [46].

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Subjects: Nutrition & Dietetics
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Ignacio Goyache
,
Deyan Yavorov-Dayliev
,
Fermín I. Milagro
,
Paula Aranaz
View Times: 61
Revisions: 2 times (View History)
Update Date: 18 Feb 2024
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