Gut Microbiota and Extreme Longevity

The study of the extreme limits of human lifespan may allow a better understanding of how human beings can escape, delay, or survive the most frequent age-related causes of morbidity, a peculiarity shown by long-living individuals. Longevity is a complex trait in which genetics, environment, and stochasticity concur to determine the chance to reach 100 or more years of age [1Cevenini E. Invidia L. Lescai F. Salvioli S. Tieri P. Castellani G. Franceschi C. Human models of aging and longevity.Expert Opin. Biol. Ther. 2008; 8: 1393-1405Crossref PubMed Scopus (116) Google Scholar]. Because of its impact on human metabolism and immunology, the gut microbiome has been proposed as a possible determinant of healthy aging [2Claesson M.J. Jeffery I.B. Conde S. Power S.E. O’Connor E.M. Cusack S. Harris H.M. Coakley M. Lakshminarayanan B. O’Sullivan O. et al.Gut microbiota composition correlates with diet and health in the elderly.Nature. 2012; 488: 178-184Crossref PubMed Scopus (2089) Google Scholar, 3Candela M. Biagi E. Brigidi P. O’Toole P.W. De Vos W.M. Maintenance of a healthy trajectory of the intestinal microbiome during aging: a dietary approach.Mech. Ageing Dev. 2014; 136-137: 70-75Crossref PubMed Scopus (55) Google Scholar]. Indeed, the preservation of host-microbes homeostasis can counteract inflammaging [4Biagi E. Nylund L. Candela M. Ostan R. Bucci L. Pini E. Nikkïla J. Monti D. Satokari R. Franceschi C. et al.Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians.PLoS ONE. 2010; 5: e10667Crossref PubMed Scopus (986) Google Scholar], intestinal permeability [5Nicoletti C. Age-associated changes of the intestinal epithelial barrier: local and systemic implications.Expert Rev. Gastroenterol. Hepatol. 2015; 9: 1467-1469Crossref PubMed Scopus (40) Google Scholar], and decline in bone and cognitive health [6Villa C.R. Ward W.E. Comelli E.M. Gut microbiota-bone axis.Crit. Rev. Food Sci. Nutr. 2015; (Published online October 13, 2015)https://doi.org/10.1080/10408398.2015.1010034Crossref PubMed Scopus (47) Google Scholar, 7Leung K. Thuret S. Gut microbiota: a modulator of brain plasticity and cognitive function in ageing.Healthcare. 2015; 3: 898-916Crossref Scopus (52) Google Scholar]. Aiming at deepening our knowledge on the relationship between the gut microbiota and a long-living host, we provide for the first time the phylogenetic microbiota analysis of semi-supercentenarians, i.e., 105–109 years old, in comparison to adults, elderly, and centenarians, thus reconstructing the longest available human microbiota trajectory along aging. We highlighted the presence of a core microbiota of highly occurring, symbiotic bacterial taxa (mostly belonging to the dominant Ruminococcaceae, Lachnospiraceae, and Bacteroidaceae families), with a cumulative abundance decreasing along with age. Aging is characterized by an increasing abundance of subdominant species, as well as a rearrangement in their co-occurrence network. These features are maintained in longevity and extreme longevity, but peculiarities emerged, especially in semi-supercentenarians, describing changes that, even accommodating opportunistic and allochthonous bacteria, might possibly support health maintenance during aging, such as an enrichment and/or higher prevalence of health-associated groups (e.g., Akkermansia, Bifidobacterium, and Christensenellaceae).