Gut Seasons: Photoperiod Effects on Fecal Microbiota in Healthy and Cafeteria-Induced Obese Fisher 344 Rats
<p>Animal experimental design. 13-week-old male STD- or CAF-fed Fischer 344 rats were pair-housed under three different photoperiods (6, 12 or 18 h of light per day) for 9 weeks. (<span class="html-italic">n</span> = 7–8). ♂: represents male sex; L6: short photoperiod (6 h light/18 h dark); L12: standard photoperiod (12 h light/12 h dark); L18: long photoperiod (18 h light/6 h dark); STD: standard chow diet; CAF: cafeteria diet.</p> "> Figure 2
<p>Effects of photoperiods on body weight gain in STD- and CAF-fed rats. (<b>a</b>) Body weight gain under short (L6), standard (L12) and long (L18) photoperiods across the 9 weeks of the experiment. * indicates significant CAF effect and <span class="html-italic">a,b</span> letters indicate significant CAF and photoperiod effects respectively, analyzed by repeated measures ANOVA followed by LSD post hoc test (<span class="html-italic">p</span> < 0.05). (<b>b</b>) Area under the curve (AUC) of body weight gain. * indicates significant CAF effect and <span class="html-italic">a,b</span> letters indicate photoperiod effect, analyzed by 2-way ANOVA followed by LSD post hoc test (<span class="html-italic">p</span> < 0.05). Data are plotted as the mean ± SD (<span class="html-italic">n</span> = 7–8). L6: short photoperiod (6 h light/18 h dark); L12: standard photoperiod (12 h light/12 h dark); L18: long photoperiod (18 h light/6 h dark); STD: standard chow diet; CAF: cafeteria diet.</p> "> Figure 3
<p>Effect of photoperiods (Ph) on both fecal microbial diversity and bacteria phyla relative abundance. Principal coordinates analysis (PCoA) 2D plot (PERMANOVA, <span class="html-italic">p</span> < 0.001) of fecal microbiota beta diversity based on Bray–Curtis distances in (<b>a</b>) STD- and in (<b>b</b>) CAF-fed rats; (<b>c</b>) alpha diversity calculated by chao-1 index in STD- and CAF-fed rats under the three different Ph conditions. Data are plotted as box and whiskers (median with interquartile ranges). * Indicates significant diet effect between STD and CAF-fed rats under same photoperiod conditions, analyzed by U-Mann–Whitney (<span class="html-italic">p</span> < 0.05); <span class="html-italic">a,b</span> letters indicate significant photoperiod effect analyzed by Kruskal–Wallis test followed by Bonferroni correction for multiple comparisons (<span class="html-italic">p</span> < 0.016); (<b>d</b>) relative abundance of different bacteria taxa at phylum level. (<span class="html-italic">n</span> = 7–8). L6: short photoperiod (6 h light/18 h dark); L12: standard photoperiod (12 h light/12 h dark); L18: long photoperiod (18 h light/6 h dark); STD: standard chow diet; CAF: cafeteria diet.</p> "> Figure 4
<p>Relative abundance at genus level of the most abundant genera significantly altered by photoperiods. Stacked bar plots showing the relative abundance of each taxa at genus level. (<span class="html-italic">n</span> = 7–8). L6: short photoperiod (6 h light/18 h dark); L12: standard photoperiod (12 h light/12 h dark); L18: long photoperiod (18 h light/6 h dark); STD: standard chow diet; CAF: cafeteria diet.</p> "> Figure 5
<p>Correlations between fecal microbiota and body weight gain and fat parameters analyzed by Spearman’s rank correlation coefficient (rho) at phylum level. Heat map with hierarchical clustering based on correlation coefficient between bacteria and biometric parameters at phylum level. Positive and negative correlations are represented in red and blue respectively. The higher the color intensity the higher the degree of correlation.</p> "> Figure 6
<p>Correlations between fecal microbiota and fat parameters analyzed by Spearman’s rank correlation coefficient (rho) at genus level. (<b>a</b>) Heat map with hierarchical clustering based on correlation coefficient between bacteria and fat parameters at genus level. Positive and negative correlations are represented in red and blue, respectively. The higher the color intensity the higher the degree of correlation. (<b>b</b>) Locally weighted linear regression (Lowess model) analysis of the strongest observed correlation in several bacteria genera affected by photoperiod.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Physical Activity Measurements
2.3. 16S rRNA Analysis
2.4. Statistical Analysis
3. Results
3.1. Photoperiod Effect on Body Weight
3.2. Photoperiods Affect Fecal Microbiota Composition: Higher Impact on Cafeteria Diet-Fed Rats
3.3. Correlations between Fecal Microbiota Taxa, Body Weight Gain and Fat Parameters
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Patterson, E.; Ryan, P.M.; Cryan, J.F.; Dinan, T.G.; Ross, R.P.; Fitzgerald, G.F.; Stanton, C. Gut microbiota, obesity and diabetes. Postgrad. Med. J. 2016, 92, 286–300. [Google Scholar] [CrossRef] [PubMed]
- Torres-Fuentes, C.; Schellekens, H.; Dinan, T.G.; Cryan, J.F. The microbiota–gut–brain axis in obesity. Lancet Gastroenterol. Hepatol. 2017, 2, 747–756. [Google Scholar] [CrossRef]
- Sandhu, K.V.; Sherwin, E.; Schellekens, H.; Stanton, C.; Dinan, T.; Cryan, J.F. Feeding the microbiota-gut-brain axis: Diet, microbiome, and neuropsychiatry. Transl. Res. 2017, 179, 223–244. [Google Scholar] [CrossRef]
- Del Chierico, F.; Vernocchi, P.; Dallapiccola, B.; Putignani, L. Mediterranean diet and health: Food effects on gut microbiota and disease control. Int. J. Mol. Sci. 2014, 15, 11678–11699. [Google Scholar] [CrossRef]
- Shi, Z. Gut microbiota: An important link between western diet and chronic diseases. Nutrients 2019, 11, 2287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Del Bas, J.M.; Guirro, M.; Boqué, N.; Cereto, A.; Ras, R.; Crescenti, A.; Caimari, A.; Canela, N.; Arola, L. Alterations in gut microbiota associated with a cafeteria diet and the physiological consequences in the host. Int. J. Obes. 2018, 42, 746–754. [Google Scholar] [CrossRef]
- Nobs, S.P.; Tuganbaev, T.; Elinav, E. Microbiome diurnal rhythmicity and its impact on host physiology and disease risk. EMBO Rep. 2019, 20, e47129. [Google Scholar] [CrossRef]
- Thaiss, C.A.; Levy, M.; Korem, T.; Dohnalová, L.; Shapiro, H.; Jaitin, D.A.; David, E.; Winter, D.; Gury-BenAri, M.; Tatirovsky, E.; et al. Microbiota Diurnal Rhythmicity Programs Host Transcriptome Oscillations. Cell 2016, 167, 1495–1510.e12. [Google Scholar] [CrossRef] [Green Version]
- Claustrat, B.; Leston, J. Melatonin: Physiological effects in humans. Neurochirurgie 2015, 61, 77–84. [Google Scholar] [CrossRef]
- Johnston, J.D.; Ordovás, J.M.; Scheer, F.A.; Turek, F.W. Circadian rhythms, metabolism, and chrononutrition in rodents and humans. Adv. Nutr. 2016, 7, 399–406. [Google Scholar] [CrossRef] [Green Version]
- Refinetti, R. Integration of biological clocks and rhythms. Compr. Physiol. 2012, 2, 1213–1239. [Google Scholar] [CrossRef] [PubMed]
- Rácz, B.; Dušková, M.; Stárka, L.; Hainer, V.; Kunešová, M. Links between the circadian rhythm, obesity and the microbiome. Physiol. Res. 2018, 67, S409–S420. [Google Scholar] [CrossRef] [PubMed]
- Onishi, K.G.; Maneval, A.C.; Cable, E.C.; Tuohy, M.C.; Scasny, A.J.; Sterina, E.; Love, J.A.; Riggle, J.P.; Malamut, L.K.; Mukerji, A.; et al. Circadian and circannual timescales interact to generate seasonal changes in immune function. Brain Behav. Immun. 2019, 83, 33–43. [Google Scholar] [CrossRef] [PubMed]
- Murphy, B.A. Circadian and Circannual Regulation in the Horse: Internal Timing in an Elite Athlete. J. Equine Veter. Sci. 2019, 76, 14–24. [Google Scholar] [CrossRef]
- Tackenberg, M.C.; McMahon, D.G. Photoperiodic Programming of the SCN and Its Role in Photoperiodic Output. Neural Plast. 2018, 2018, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Coomans, C.; Ramkisoensing, A.; Meijer, J.H. The suprachiasmatic nuclei as a seasonal clock. Front. Neuroendocr. 2015, 37, 29–42. [Google Scholar] [CrossRef]
- Haus, E. Chronobiology in the endocrine system. Adv. Drug Deliv. Rev. 2007, 59, 985–1014. [Google Scholar] [CrossRef]
- Vitale, J.A.; Briguglio, M.; Galentino, R.; Dell’Osso, B.; Malgaroli, A.; Banfi, G.; Porta, M. Exploring circannual rhythms and chronotype effect in patients with Obsessive-Compulsive Tic Disorder (OCTD): A pilot study. J. Affect. Disord. 2020, 262, 286–292. [Google Scholar] [CrossRef]
- Jin, J.; Yaegashi, T.; Hashizume, T. Effects of photoperiod on the secretion of growth hormone and prolactin during nighttime in female goats. Anim. Sci. J. 2013, 84, 130–135. [Google Scholar] [CrossRef]
- Mariné-Casadó, R.; Coca, C.D.; Del Bas, J.M.; Bladé, C.; Arola, L.; Caimari, A. The exposure to different photoperiods strongly modulates the glucose and lipid metabolisms of normoweight fischer 344 rats. Front. Physiol. 2018, 9, 416. [Google Scholar] [CrossRef]
- Bailey, M.T.; Walton, J.C.; Dowd, S.; Weil, Z.; Nelson, R.J. Photoperiod modulates gut bacteria composition in male Siberian hamsters (Phodopus sungorus). Brain Behav. Immun. 2010, 24, 577–584. [Google Scholar] [CrossRef]
- Davenport, E.; Mizrahi-Man, O.; Michelini, K.; Barreiro, L.; Ober, C.; Gilad, Y. Seasonal variation in human gut microbiome composition. PLoS ONE 2014, 9, e90731. [Google Scholar] [CrossRef]
- Shor, E.K.; Brown, S.P.; Freeman, D.A. A novel role for the pineal gland: Regulating seasonal shifts in the gut microbiota of Siberian hamsters. J. Pineal Res. 2020, 69, e12696. [Google Scholar] [CrossRef] [PubMed]
- Fan, C.; Zhang, L.; Jia, S.; Tang, X.; Fu, H.; Li, W.; Liu, C.; Zhang, H.; Cheng, Q.; Zhang, Y. Seasonal variations in the composition and functional profiles of gut microbiota reflect dietary changes in plateau pikas. Integr. Zool. 2022. [Google Scholar] [CrossRef] [PubMed]
- Huang, G.; Wang, L.; Li, J.; Hou, R.; Wang, M.; Wang, Z.; Qu, Q.; Zhou, W.; Nie, Y.; Hu, Y.; et al. Seasonal shift of the gut microbiome synchronizes host peripheral circadian rhythm for physiological adaptation to a low-fat diet in the giant panda. Cell Rep. 2022, 38, 110203. [Google Scholar] [CrossRef]
- Yang, X.; Yao, Y.; Zhang, X.; Zhong, J.; Gao, F.; Zhang, H.; Han, Y.; Weng, Q.; Yuan, Z. Seasonal Changes in the Distinct Taxonomy and Function of the Gut Microbiota in the Wild Ground Squirrel (Spermophilus dauricus). Animals 2021, 11, 2685. [Google Scholar] [CrossRef]
- Jiang, F.; Gao, H.; Qin, W.; Song, P.; Wang, H.; Zhang, J.; Liu, D.; Wang, D.; Zhang, T. Marked Seasonal Variation in Structure and Function of Gut Microbiota in Forest and Alpine Musk Deer. Front. Microbiol. 2021, 12, 2460. [Google Scholar] [CrossRef] [PubMed]
- Huang, C.; Liao, W. Seasonal variation in gut microbiota related to diet in Fejervarya limnocharis. Animals 2021, 11, 1393. [Google Scholar] [CrossRef] [PubMed]
- Wu, G.; Tang, W.; He, Y.; Hu, J.; Gong, S.; He, Z.; Wei, G.; Lv, L.; Jiang, Y.; Zhou, H.; et al. Light exposure influences the diurnal oscillation of gut microbiota in mice. Biochem. Biophys. Res. Commun. 2018, 501, 16–23. [Google Scholar] [CrossRef]
- Oyola, M.G.; Johnson, R.C.; Bauman, B.M.; Frey, K.G.; Russell, A.L.; Cho-Clark, M.; Buban, K.N.; Bishop-Lilly, K.A.; Merrell, D.S.; Handa, R.J.; et al. Gut microbiota and metabolic marker alteration following dietary isoflavone-photoperiod interaction. Endocrinol. Diabetes Metab. 2021, 4, e00190. [Google Scholar] [CrossRef]
- Ávila-Román, J.; Arreaza-Gil, V.; Cortés-Espinar, A.J.; Soliz-Rueda, J.R.; Mulero, M.; Muguerza, B.; Arola-Arnal, A.; Arola, L.; Torres-Fuentes, C. Impact of gut microbiota on plasma oxylipins profile under healthy and obesogenic conditions. Clin. Nutr. 2021, 40, 1475–1486. [Google Scholar] [CrossRef] [PubMed]
- Dhariwal, A.; Chong, J.; Habib, S.; King, I.L.; Agellon, L.B.; Xia, J. MicrobiomeAnalyst: A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 2017, 45, W180–W188. [Google Scholar] [CrossRef] [PubMed]
- Chong, J.; Liu, P.; Zhou, G.; Xia, J. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat. Protoc. 2020, 15, 799–821. [Google Scholar] [CrossRef]
- Voreades, N.; Kozil, A.; Weir, T.L. Diet and the development of the human intestinal microbiome. Front. Microbiol. 2014, 5, 494. [Google Scholar] [CrossRef] [Green Version]
- Gibson, M.K.; Crofts, T.S.; Dantas, G. Antibiotics and the developing infant gut microbiota and resistome. Curr. Opin. Microbiol. 2015, 27, 51–56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Coman, V.; Vodnar, D.C. Gut microbiota and old age: Modulating factors and interventions for healthy longevity. Exp. Gerontol. 2020, 141, 111095. [Google Scholar] [CrossRef]
- Kim, Y.S.; Unno, T.; Kim, B.-Y.; Park, M.-S. Sex Differences in Gut Microbiota. World J. Mens Health 2020, 38, 48–60. [Google Scholar] [CrossRef]
- O’Sullivan, O.; Cronin, O.; Clarke, S.F.; Murphy, E.F.; Molloy, M.G.; Shanahan, F.; Cotter, P. Exercise and the microbiota. Gut Microbes 2015, 6, 131–136. [Google Scholar] [CrossRef] [Green Version]
- Rea, K.; Dinan, T.; Cryan, J.F. The microbiome: A key regulator of stress and neuroinflammation. Neurobiol. Stress 2016, 4, 23–33. [Google Scholar] [CrossRef] [Green Version]
- Ren, C.C.; Sylvia, K.E.; Munley, K.M.; Deyoe, J.E.; Henderson, S.G.; Vu, M.P.; Demas, G.E. Photoperiod modulates the gut microbiome and aggressive behavior in Siberian hamsters. J. Exp. Biol. 2020, 223, jeb212548. [Google Scholar] [CrossRef]
- Macedo, I.C.; de Freitas, J.S.; Torres, I.L.D.S. The influence of palatable diets in reward system activation: A mini review. Adv. Pharmacol. Sci. 2016, 2016, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guirro, M.; Costa, A.; Gual-Grau, A.; Herrero, P.; Torrell, H.; Canela, N.; Arola, L. Effects from diet-induced gut microbiota dysbiosis and obesity can be ameliorated by fecal microbiota transplantation: A multiomics approach. PLoS ONE 2019, 14, e0218143. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Le Chatelier, E.; Nielsen, T.; Qin, J.; Prifti, E.; Hildebrand, F.; Falony, G.; Almeida, M.; Arumugam, M.; Batto, J.-M.; Kennedy, S.; et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013, 500, 541–546. [Google Scholar] [CrossRef]
- Zhang, C.; Zhang, M.; Pang, X.; Zhao, Y.; Wang, L.; Zhao, L. Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J. 2012, 6, 1848–1857. [Google Scholar] [CrossRef]
- Gual-Grau, A.; Guirro, M.; Mayneris-Perxachs, J.; Arola, L.; Boqué, N. Impact of different hypercaloric diets on obesity features in rats: A metagenomics and metabolomics integrative approach. J. Nutr. Biochem. 2019, 71, 122–131. [Google Scholar] [CrossRef] [PubMed]
- Devkota, S.; Wang, Y.; Musch, M.W.; Leone, V.; Fehlner-Peach, H.; Nadimpalli, A.; Antonopoulos, D.A.; Jabri, B.; Chang, E.B. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012, 487, 104–108. [Google Scholar] [CrossRef] [Green Version]
- Magne, F.; Gotteland, M.; Gauthier, L.; Zazueta, A.; Pesoa, S.; Navarrete, P.; Balamurugan, R. The firmicutes/bacteroidetes ratio: A relevant marker of gut dysbiosis in obese patients? Nutrients 2020, 12, 1474. [Google Scholar] [CrossRef] [PubMed]
- Crovesy, L.; Masterson, D.; Rosado, E.L. Profile of the gut microbiota of adults with obesity: A systematic review. Eur. J. Clin. Nutr. 2020, 74, 1251–1262. [Google Scholar] [CrossRef]
- Deaver, J.A.; Eum, S.Y.; Toborek, M. Circadian disruption changes gut microbiome taxa and functional gene composition. Front. Microbiol. 2018, 9, 737. [Google Scholar] [CrossRef]
- Goldman, B.D. Mammalian photoperiodic system: Formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J. Biol. Rhythm. 2001, 16, 283–301. [Google Scholar] [CrossRef]
- Varpe, O.H. Life History Adaptations to Seasonality. In Integrative and Comparative Biology; Oxford University Press: Oxford, UK, 2017; Volume 57, pp. 943–960. [Google Scholar] [CrossRef] [Green Version]
- Hut, R.A.; Beersma, D.G.M. Evolution of time-keeping mechanisms: Early emergence and adaptation to photoperiod. Philos. Trans. R. Soc. B Biol. Sci. 2011, 366, 2141–2154. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jumpertz, R.; Le, D.S.; Turnbaugh, P.J.; Trinidad, C.; Bogardus, C.; Gordon, J.I.; Krakoff, J. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 2011, 94, 58–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bäckhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004, 101, 15718–15723. [Google Scholar] [CrossRef] [Green Version]
- Ramakrishna, B. Role of the gut microbiota in human nutrition and metabolism. J. Gastroenterol. Hepatol. 2013, 28, 9–17. [Google Scholar] [CrossRef]
- Samuel, B.S.; Shaito, A.; Motoike, T.; Rey, F.E.; Backhed, F.; Manchester, J.K.; Hammer, R.E.; Williams, S.C.; Crowley, J.; Yanagisawa, M.; et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc. Natl. Acad. Sci. USA 2008, 105, 16767–16772. [Google Scholar] [CrossRef] [Green Version]
- Ottman, N.; Smidt, H.; De Vos, W.M.; Belzer, C. The function of our microbiota: Who is out there and what do they do? Front. Cell. Infect. Microbiol. 2012, 2, 104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raman, M.; Ahmed, I.; Gillevet, P.M.; Probert, C.S.; Ratcliffe, N.M.; Smith, S.; Greenwood, R.; Sikaroodi, M.; Lam, V.; Crotty, P.; et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin. Gastroenterol. Hepatol. 2013, 11, 868–875.e3. [Google Scholar] [CrossRef] [PubMed]
- Zarrinpar, A.; Chaix, A.; Yooseph, S.; Panda, S. Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 2014, 20, 1006–1017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, Z.; Yin, J.; Zhang, J.; Ward, R.E.; Martin, R.J.; Lefevre, M.; Cefalu, W.T.; Ye, J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009, 58, 1509–1517. [Google Scholar] [CrossRef] [Green Version]
- Mariné-Casadó, R.; Domenech-Coca, C.; Del Bas, J.M.; Bladé, C.; Arola, L.; Caimari, A. Intake of an Obesogenic Cafeteria Diet Affects Body Weight, Feeding Behavior, and Glucose and Lipid Metabolism in a Photoperiod-Dependent Manner in F344 Rats. Front. Physiol. 2018, 9, 1–16. [Google Scholar] [CrossRef]
- Shoemaker, M.B.; Heideman, P.D. Reduced body mass, food intake, and testis size in response to short photoperiod in adult F344 rats. BMC Physiol. 2002, 2, 11. [Google Scholar] [CrossRef] [PubMed]
- Tavolaro, F.M.; Thomson, L.M.; Ross, A.; Morgan, P.; Helfer, G. Photoperiodic Effects on Seasonal Physiology, Reproductive Status and Hypothalamic Gene Expression in Young Male F344 Rats. J. Neuroendocr. 2015, 27, 79–87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heideman, P.D.; Sylvester, C.J. Reproductive Photoresponsiveness in Unmanipulated Male Fischer 344 Laboratory Rats1. Biol. Reprod. 1997, 57, 134–138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Arreaza-Gil, V.; Escobar-Martínez, I.; Suárez, M.; Bravo, F.I.; Muguerza, B.; Arola-Arnal, A.; Torres-Fuentes, C. Gut Seasons: Photoperiod Effects on Fecal Microbiota in Healthy and Cafeteria-Induced Obese Fisher 344 Rats. Nutrients 2022, 14, 722. https://doi.org/10.3390/nu14030722
Arreaza-Gil V, Escobar-Martínez I, Suárez M, Bravo FI, Muguerza B, Arola-Arnal A, Torres-Fuentes C. Gut Seasons: Photoperiod Effects on Fecal Microbiota in Healthy and Cafeteria-Induced Obese Fisher 344 Rats. Nutrients. 2022; 14(3):722. https://doi.org/10.3390/nu14030722
Chicago/Turabian StyleArreaza-Gil, Verónica, Iván Escobar-Martínez, Manuel Suárez, Francisca Isabel Bravo, Begoña Muguerza, Anna Arola-Arnal, and Cristina Torres-Fuentes. 2022. "Gut Seasons: Photoperiod Effects on Fecal Microbiota in Healthy and Cafeteria-Induced Obese Fisher 344 Rats" Nutrients 14, no. 3: 722. https://doi.org/10.3390/nu14030722