Multi-omics gut microbiome signatures in obese women: role of diet and uncontrolled eating behavior
Monica Barone,
Silvia Garelli,
Simone Rampelli,
Alessandro Agostini,
Silke Matysik,
Federica D’Amico,
Sabrina Krautbauer,
Roberta Mazza,
Nicola Salituro,
Flaminia Fanelli,
Patricia Iozzo,
Yolanda Sanz,
Marco Candela,
Patrizia Brigidi,
Uberto Pagotto,
Silvia Turroni
Affiliations
Monica Barone
Microbiomics Unit, Department of Medical and Surgical Sciences, University of Bologna
Silvia Garelli
Unit of Endocrinology and Prevention and Care of Diabetes, Center for Applied Biomedical Research, S. Orsola Polyclinic, Istituto Di Ricovero E Cure a Carattere Scientifico (IRCCS), Department of Medical and Surgical Sciences, University of Bologna
Simone Rampelli
Unit of Microbiome Science and Biotechnology, Department of Pharmacy and Biotechnology, University of Bologna
Alessandro Agostini
Department of Experimental, Diagnostic, and Specialty Medicine, S. Orsola Polyclinic, Istituto Di Ricovero E Cure a Carattere Scientifico (IRCCS), University of Bologna
Silke Matysik
Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg
Federica D’Amico
Microbiomics Unit, Department of Medical and Surgical Sciences, University of Bologna
Sabrina Krautbauer
Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg
Roberta Mazza
Unit of Endocrinology and Prevention and Care of Diabetes, Center for Applied Biomedical Research, S. Orsola Polyclinic, Istituto Di Ricovero E Cure a Carattere Scientifico (IRCCS), Department of Medical and Surgical Sciences, University of Bologna
Nicola Salituro
Unit of Endocrinology and Prevention and Care of Diabetes, Center for Applied Biomedical Research, S. Orsola Polyclinic, Istituto Di Ricovero E Cure a Carattere Scientifico (IRCCS), Department of Medical and Surgical Sciences, University of Bologna
Flaminia Fanelli
Unit of Endocrinology and Prevention and Care of Diabetes, Center for Applied Biomedical Research, S. Orsola Polyclinic, Istituto Di Ricovero E Cure a Carattere Scientifico (IRCCS), Department of Medical and Surgical Sciences, University of Bologna
Patricia Iozzo
Institute of Clinical Physiology, National Research Council
Yolanda Sanz
Microbial Ecology, Nutrition & Health Research Unit, Institute of Agrochemistry and Food Technology, Spanish National Research Council (IATA-CSIC)
Marco Candela
Unit of Microbiome Science and Biotechnology, Department of Pharmacy and Biotechnology, University of Bologna
Patrizia Brigidi
Microbiomics Unit, Department of Medical and Surgical Sciences, University of Bologna
Uberto Pagotto
Unit of Endocrinology and Prevention and Care of Diabetes, Center for Applied Biomedical Research, S. Orsola Polyclinic, Istituto Di Ricovero E Cure a Carattere Scientifico (IRCCS), Department of Medical and Surgical Sciences, University of Bologna
Silvia Turroni
Unit of Microbiome Science and Biotechnology, Department of Pharmacy and Biotechnology, University of Bologna
Abstract Background Obesity and related co-morbidities represent a major health challenge nowadays, with a rapidly increasing incidence worldwide. The gut microbiome has recently emerged as a key modifier of human health that can affect the development and progression of obesity, largely due to its involvement in the regulation of food intake and metabolism. However, there are still few studies that have in-depth explored the functionality of the human gut microbiome in obesity and even fewer that have examined its relationship to eating behaviors. Methods In an attempt to advance our knowledge of the gut-microbiome-brain axis in the obese phenotype, we thoroughly characterized the gut microbiome signatures of obesity in a well-phenotyped Italian female cohort from the NeuroFAST and MyNewGut EU FP7 projects. Fecal samples were collected from 63 overweight/obese and 37 normal-weight women and analyzed via a multi-omics approach combining 16S rRNA amplicon sequencing, metagenomics, metatranscriptomics, and lipidomics. Associations with anthropometric, clinical, biochemical, and nutritional data were then sought, with particular attention to cognitive and behavioral domains of eating. Results We identified four compositional clusters of the gut microbiome in our cohort that, although not distinctly associated with weight status, correlated differently with eating habits and behaviors. These clusters also differed in functional features, i.e., transcriptional activity and fecal metabolites. In particular, obese women with uncontrolled eating behavior were mostly characterized by low-diversity microbial steady states, with few and poorly interconnected species (e.g., Ruminococcus torques and Bifidobacterium spp.), which exhibited low transcriptional activity, especially of genes involved in secondary bile acid biosynthesis and neuroendocrine signaling (i.e., production of neurotransmitters, indoles and ligands for cannabinoid receptors). Consistently, high amounts of primary bile acids as well as sterols were found in their feces. Conclusions By finding peculiar gut microbiome profiles associated with eating patterns, we laid the foundation for elucidating gut-brain axis communication in the obese phenotype. Subject to confirmation of the hypotheses herein generated, our work could help guide the design of microbiome-based precision interventions, aimed at rewiring microbial networks to support a healthy diet-microbiome-gut-brain axis, thus counteracting obesity and related complications.
