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Differences in Gut Microbiome Composition Between Senior Orienteering Athletes and Community-Dwelling Older Adults

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Differences in Gut Microbiome Composition Between Senior Orienteering Athletes and Community-Dwelling Older Adults nutrients Article Differences in Gut Microbiome Composition between Senior Orienteering Athletes and Community-Dwelling Older Adults 1, 1, 1 1 Frida Fart y, Sukithar Kochappi Rajan y, Rebecca Wall , Ignacio Rangel , 1,2 1 1 1, John Peter Ganda-Mall , Lina Tingö , Robert J. Brummer , Dirk Repsilber z, 1, 1, , Ida Schoultz z and Carl Mårten Lindqvist * z 1 School of Medical Sciences, Faculty of Medicine and Health, Örebro University, 702 81 Örebro, Sweden; [email protected] (F.F.); [email protected] (S.K.R.); [email protected] (R.W.); [email protected] (I.R.); [email protected] (J.P.G.-M.); [email protected] (L.T.); [email protected] (R.J.B.); [email protected] (D.R.); [email protected] (I.S.) 2 Laboratory of Translational Mucosal Immunology, Digestive Diseases Research Unit, Vall d’Hebron Institut de Recerca, Hospital Universitari Vall d’Hebron, 08035 Barcelona, Spain * Correspondence: [email protected] Authors contributed equally to this work. y Shared senior authorship. z Received: 18 July 2020; Accepted: 18 August 2020; Published: 27 August 2020 Abstract: Background: Gastrointestinal (GI) health is an important aspect of general health. Gastrointestinal symptoms are of specific importance for the elderly, an increasing group globally. Hence, promoting the elderly’s health and especially gastrointestinal health is important. Gut microbiota can influence gastrointestinal health by modulation of the immune system and the gut–brain axis. Diverse gut microbiota have been shown to be beneficial; however, for the elderly, the gut microbiota is often less diverse. Nutrition and physical activity, in particular, are two components that have been suggested to influence composition or diversity. Materials and Methods: In this study, we compared gut microbiota between two groups of elderly individuals: community-dwelling older adults and physically active senior orienteering athletes, where the latter group has less gastrointestinal symptoms and a reported better well-being. With this approach, we explored if certain gut microbiota were related to healthy ageing. The participant data and faecal samples were collected from these two groups and the microbiota was whole-genome sequenced and taxonomically classified with MetaPhlAn. Results: The physically active senior orienteers had a more homogeneous microbiota within the group and a higher abundance of Faecalibacterium prausnitzii compared to the community-dwelling older adults. Faecalibacterium prausnitzii has previously shown to have beneficial properties. Senior orienteers also had a lower abundance of Parasutterella excrementihominis and Bilophila unclassified, which have been associated with impaired GI health. We could not observe any difference between the groups in terms of Shannon diversity index. Interestingly, a subgroup of community-dwelling older adults showed an atypical microbiota profile as well as the parameters for gastrointestinal symptoms and well-being closer to senior orienteers. Conclusions: Our results suggest specific composition characteristics of healthy microbiota in the elderly, and show that certain components of nutrition as well as psychological distress are not as tightly connected with composition or diversity variation in faecal microbiota samples. Keywords: gut microbiota; metagenomics; aged; Faecalibacterium prausnitzii; orienteering Nutrients 2020, 12, 2610; doi:10.3390/nu12092610 www.mdpi.com/journal/nutrients Nutrients 2020, 12, 2610 2 of 17 Nutrients 2020, 11, x 2 of 19 1.1. Introduction Introduction DuringDuring the lastlast decade,decade, longevity longevity has has increased increased among among the elderlythe elderly population, population resulting, resulting in a global in a globalageing ageing phenomenon phenomenon that is that having is having a major a major impact impact on healthcare on health systemscare systems worldwide. worldwide. This has This led has to ledan increasedto an increased awareness awareness of the importance of the importance of promoting of promot healthying ageing healthy and ageing quality and of lifequality throughout of life throughoutan individual’s an individual lifespan. To’s promotelifespan. andTo promote initiate healthy and initiate ageing, healthy it is important ageing, toit understandis important and to understandreveal the underlying and reveal mechanisms. the underlying mechanisms. TheThe gastrointestinal gastrointestinal (GI) (GI) tract tract is is an an essential essential part part of of the the human body and physiological system system throughthrough whichwhich health health and and well-being well-being might might be promoted be promoted [1]. A well-functioning[1]. A well-functioning GI tract hasGI previouslytract has previouslybeen identified been as identified crucial for as subjective crucial for health subjective and well-being health and among well-being older adultsamong [ 2older]. GI symptomsadults [2]. areGI symptomscommon among are common community-dwelling among community older-dwelling adults (i.e., older older adults adults (i.e. residing, older inadults their residing own household) in their ownin Sweden, household) and as in many Sweden as 65%, and experience as many one as or65% several experience gut symptoms one or several that correlate gut symptoms with increased that correlatepsychological with distress, increased including psychological anxiety anddistress, depression including [3]. On anxiety the contrary, and depression physically active[3]. On seniors the contrary,engaged inphysically orienteering active (a sportseniors involving engaged finding in orienteering specific locations (a sport using involving a map finding and a compass)specific locationshave previously using a map been and identified a compass) as a potentialhave previously model ofbeen healthy identified ageing as [a4 potential], as they model display of the healthy three ageingmain components [4], as they of display successful the ageing—physicalthree main components endurance, of s cognitiveuccessful skills,ageing and—physical social interaction endurance, [5]. cognIndeed,itive our skills previous, and social data interaction show fewer [5]. GI Indeed, symptoms our previous among data senior show orienteers fewer GI and symptoms a better among overall seniorhealth orienteers compared and to community-dwelling a better overall health older compared adults to [4 community,6]. This indicates-dwelling that older gut health adults may [4,6] reveal. This indicatesimportant that factors gut health of well-being may reveal in the important elderly, especiallyfactors of itswell association-being in the with elderly, various especially factors that its associationare known with to influence various gutfactors microbiota that are known during to the influence entire lifespan. gut microbiota The microbial during the composition entire lifespan. of an Theindividual microbial depends composition on factors of such an asindividual age, diet, geography,depends on environmental factors such exposure,as age, diet, and manygeography, others, environmentalas shown in Figure exposure1[7–10, and]. many others, as shown in Figure 1 [7–10]. Figure 1. Factors affecting the composition of gut microbiota. The human GI tract is a complex ecosystem where the gut microbiome interplays with host cells and dietary-derivedFigure components, 1. Factors affecting both of the which composition have been of gut implicated microbiota. in playing a major role in health and disease [1]. A diverse gut microbiome has been related to several essential mechanisms The human GI tract is a complex ecosystem where the gut microbiome interplays with host cells for both a well-functioning GI tract as well as well-being, including modulating the immune system, and dietary-derived components, both of which have been implicated in playing a major role in maintaining an intact intestinal barrier, and being a part of the regulation of the gut-brain axis [11,12], health and disease [1]. A diverse gut microbiome has been related to several essential mechanisms where a decreased diversity has been linked to both GI and psychiatric disorders [13]. Ageing has been for both a well-functioning GI tract as well as well-being, including modulating the immune system, associated with a loss of diversity of the gut microbiome; specifically, bacteria belonging to the phyla maintaining an intact intestinal barrier, and being a part of the regulation of the gut-brain axis [11,12], Firmicutes and Actinobacteria decrease, whereas Proteobacteria increase in abundance [14]. These changes where a decreased diversity has been linked to both GI and psychiatric disorders [13]. Ageing has could be due to nutritional deficiencies such as lower intakes of specific nutrients, e.g., dietary fibres been associated with a loss of diversity of the gut microbiome; specifically, bacteria belonging to the and proteins, that are important for maintaining the immune and GI functions [15]. Recent evidence phyla Firmicutes and Actinobacteria decrease, whereas Proteobacteria increase in abundance [14]. These changes could be due to nutritional deficiencies such as lower intakes of specific nutrients, e.g., Nutrients 2020, 12, 2610 3 of 17 further indicates that physical activity, independent of diet, could induce positive alterations of the gut microbiome composition [16,17]. However, the relationship between physical activity and gut microbiota across the life course has not been entirely elucidated. It is also less known to what extent microbiome composition and diversity
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