Physical activity shifts gut microbiota structure in aged subjects with overweight/obesity and metabolic syndrome

Patricia Ruiz-Limón; Jananee Muralidharan; Ana M Gomez-Perez; Mora Murri; Jesús Vioque; Dolores Corella; Montse Fitó; Josep Vidal; Jordi Salas-Salvadó; Laura Torres-Collado; Oscar Coltell; Alessandro Atzeni; Olga Castañer; Mònica Bulló; M Rosa Bernal-López; Isabel Moreno-Indias; Francisco J Tinahones

doi:10.5114/biolsport.2024.133005

Physical activity shifts gut microbiota structure in aged subjects with overweight/obesity and metabolic syndrome

Biol Sport. 2024 Jul;41(3):47-60. doi: 10.5114/biolsport.2024.133005. Epub 2023 Dec 20.

Authors

Patricia Ruiz-Limón^{1

2}, Jananee Muralidharan^{2

3}, Ana M Gomez-Perez^{1

2}, Mora Murri^{1

2}, Jesús Vioque^{4

5}, Dolores Corella^{2

6}, Montse Fitó^{2

7}, Josep Vidal^{8

9}, Jordi Salas-Salvadó^{2

3

10}, Laura Torres-Collado^{4

5}, Oscar Coltell¹¹, Alessandro Atzeni^{2

3}, Olga Castañer^{2

7}, Mònica Bulló^{2

3}, M Rosa Bernal-López^{2

12}, Isabel Moreno-Indias^{1

2}, Francisco J Tinahones^{1

2}

Affiliations

¹ Department of Endocrinology and Nutrition, Virgen de la Victoria University Hospital, The Biomedical Research Institute of Malaga and Platform in Nanomedicine (IBIMA BIONAND Platform), University of Malaga, 29016 Malaga, Spain.
² CIBER in Physiopathology of Obesity and Nutrition (CIBEROBN), Carlos III Health Institute, 28029 Madrid, Spain.
³ University of Rovira i Virgili, Department of Biochemistry and Biotechnology, Human Nutrition Unit, 43003 Reus, Spain.
⁴ Institute of Health and Biomedical Research of Alicante. University of Miguel Hernández (ISABIAL-UMH), 03010 Alicante, Spain.
⁵ CIBER Epidemiology and Public Health (CIBERESP), Carlos III Health Institute, 28029 Madrid, Spain.
⁶ Department of Preventive Medicine, University of Valencia, 46100 Valencia, Spain.
⁷ Cardiovascular Risk and Nutrition (Regicor Study Group), Hospital del Mar Research Institute (IMIM), 08003 Barcelona, Spain.
⁸ Endocrinology and Nutrition Department, Clinic Universitary Hospital, 08036 Barcelona, Spain.
⁹ August Pi i Sunyer Biomedical Research Institute (IDIBAPS), 08036 Barcelona, Spain.
¹⁰ Pere i Virgili Health Research Institute (IISPV). San Joan University Hospital, 43003 Reus, Spain.
¹¹ Department of Computer Sciences. University Jaume I, Castellon, Spain.
¹² Department of Internal Medicine of Regional University Hospital, Institute of Biomedical Research in Malaga (IBIMA), 29009 Málaga, Spain.

Abstract

We aimed to identify how physical activity (PA), within the context of a Mediterranean diet, affects metabolic variables and gut microbiota in older individuals with overweight/obesity and metabolic syndrome. Observational analysis was conducted as part of the PREDIMED-Plus study with 152 males and 145 females with overweight/obesity and metabolic syndrome. General assessments, anthropometric and biochemical measurements, and gut microbial 16S rRNA sequencing data were analyzed at baseline and 1-year of follow-up. Participants were stratified by tertiles of 1-year change in total PA-related energy expenditure ranging from -98.77 to 1099.99 METs (min/week). The total PA percentage of change was reduced in tertile 1 (-44.83 ± 24.94), increased in tertile 2 (28.96 ± 23.33) and tertile 3 (273.64 ± 221.42). Beta diversity analysis showed differences in the gut microbiota population within each tertile group. Significant differences were found at phylum, family, and genus levels in the gut microbiota of the three tertile groups at baseline and 1-year timepoint. Tertile 3, the group with the greatest increase in PA, was characterized by increases in their levels of Sutterella, Bilophila, and Lachnospira bacteria as well as a reduction in Collinsella. Moreover, this tertile showed a different pattern in its predicted metabolic capacities to the other groups. Our results have demonstrated that changes in PA such as lifestyle and Mediterranean diet induces specific variations in the gut microbiota profile. This modulation of gut microbiome populations and their metabolic capacities may contribute to the health of the aged individuals with overweight/obesity and metabolic syndrome.

Keywords: Gut microbiota; Metabolic syndrome; Obesity; Overweight; Physical activity.

Grants and funding

Funding sources This work was supported by the official Spanish Institutions for funding scientific biomedical research, CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN) and Instituto de Salud Carlos III (ISCIII), through the Fondo de Investigación para la Salud (FIS), which is co-funded by the European Regional Development Fund (three coordinated FIS projects lead by JS-S: PI13/00462, PI16/00501 and PI19/00576; two led by JV: PI17/01441, PI14/01206; and two led by MRBL: PI14/00696 and PI17/00855); the Especial Action Project entitled: Implementación y evaluación de una intervención intensiva sobre la actividad física Cohorte PREDIMED-Plus grant (OBN16PE01) to JS-S; the Recercaixa (number 2013ACUP00194) grant to JS-S. DC obtained grant from the Generalitat Valenciana (PROMETEO 2017/17) and Grant from the Ministry of Science and Innovation/Instituto de Salud Carlos III (reference: PI19/00781). Eat2beNICE project (European Union’s Horizon 2020 research and innovation programme under grant agreement No 728018). PRL was supported by a “Sara Borrell” postdoctoral contract (CD19/00216) from the ISCIII-Madrid (Spain), co-financed by the Fondo Europeo de Desarrollo Regional-(FEDER). IMI was supported by the “Miguel Servet Type II” program (CPII21/00013) of the ISCIII-Madrid (Spain), co-financed by the FEDER. JM and AA were supported by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 713679, cofunded from the Universitat Rovira i Virgili (URV) and Fundació Catalunya La Pedrera. OCN was supported by Juan Rodés program JR17/00022 and PI20/00012. MM is supported by Miguel Servet I program (CP17/00133) from ISCIII and cofunded by FEDER. AMGP was supported by a research contract from Servicio Andaluz de Salud (B-0033–2014). MRBL is supported by Miguel Servet II program (CPII/00014) from ISCIII and by Nicolás Monardes program (C1-0005-2020) from Servicio Andaluz de Salud, both cofunded by FEDER. This work is partially supported by ICREA. Food companies Hojiblanca (Lucena, Spain) and Patrimonio Comunal Olivarero (Madrid, Spain) donated extra virgin olive oil; and the Almond Board of California (Modesto, CA, USA), American Pistachio Growers (Fresno, CA, USA), and Paramount Farms (Wonderful Company, LLC, Los Angeles, CA, USA) donated nuts for the PREDIMED-Pilot study.