Intestinal microbiota of indigenous peoples of the North: a systematic review
- Authors: Sivtseva T.M.1, Stepanova M.A.1, Zakharova R.N.1, Semenov S.I.1, Osakovsky V.L.1
-
Affiliations:
- North-Eastern Federal University named after M.K. Ammosov
- Issue: Vol 31, No 5 (2024)
- Pages: 337-351
- Section: REVIEWS
- Submitted: 29.07.2024
- Accepted: 07.11.2024
- Published: 08.02.2025
- URL: https://hum-ecol.ru/1728-0869/article/view/634678
- DOI: https://doi.org/10.17816/humeco634678
- ID: 634678
Cite item
Abstract
BACKGROUND: The microbiota of the indigenous population of the North may play a pivotal role in the development of the polar (northern) type of metabolism supporting increased energy demands and maintaining body homeostasis in extreme cold climates. However, this area remains relatively understudied. Sequencing of bacterial 16S rRNA allows for establishing the full taxonomic composition of microbial communities, thereby facilitating novel insights into the interplay between microbiota, environmental conditions, and the formation of health in different populations.
AIM: The aim of this review is to evaluate the factors and principles of microbiota development in extreme climatic conditions and its potential impact on health in the indigenous peoples of the North.
MATERIALS AND METHODS: A systematic review was conducted based on the 2020 PRISMA guidelines. Original studies were searched for across the PubMed, eLibrary, and Google Scholar databases using Russian keywords “микробиота кишечника” (“intestinal microbiota”), “Север” (“North”), and English “gut microbiome,” “16S rRNA,” and “Arctic.”
RESULTS: Having filtered the results of the primary selection of articles in accordance with the search criteria, five publications were identified that presented the results of intestinal microbiota 16S rRNA studies in Canadian Inuit, Alaska Natives, and Yakuts of the Sakha Republic (Yakutia). The intestinal microbiota of native residents of the North differs is characterized by inter- and intra-population variability in the diversity and taxonomic composition. Despite similar climatic conditions and dietary patterns, microbiota composition of different Northern populations reflects differences in traditional activities, dietary habits, and surrounding animals.
CONCLUSION: Results of available studies are insufficient to form a comprehensive understanding of the northern microbiome and its role in maintaining the health of the indigenous peoples of the North. Nevertheless, the composition of the intestinal microbiota of the northern populations is shown to be diverse and favorable for the metabolic health; further studies are required to identify the mechanisms of the metabolic health formation in cold climate conditions.
Keywords
Full Text
Background
The relationship between gut microbiota, environmental conditions, and human health has been actively studied in recent years thanks to the development of modern methods for 16S rRNA sequencing of bacteria. Studies showed that diet, living conditions, and ethnicity had the greatest influence on the diversity and composition of gut bacteria [1–4]. These relationships are based on metabolic pathways formed by complex functional interactions between the microbial community, regulatory systems of the host organism, and the environment.
The main substrates for metabolism by microorganisms in the large intestine include complex polysaccharides and proteins that are stable and poorly absorbed in the small intestine. Anaerobic fermentation of simple carbohydrates formed during the hydrolysis of polysaccharides produces short-chain fatty acids (SCFAs), such as acetate, propionate, and butyrate, with the first of them being the most abundant product of gut microbiota. SCFAs are crucial for maintaining intestinal barrier function and can be used as an energy source [5]. The most studied positive effect is that of butyrate, which has anti-inflammatory, antioxidant, and antitumor properties. Acetate is less studied; however, it is known to be used as a metabolite for other tissues in the body and have a positive effect on the protective functions of the intestine [6]. Gut microbiota can also produce harmful products. For example, phenol, hydrogen sulfide, isobutyric acid, and isovaleric acid can be formed from amino acids during anaerobic fermentation of proteins. Metabolites of branched-chain fatty acid fermentation also produce substances that can negatively affect the health of the host and cause ulcers, colitis, or cancer [7].
In the era witnessing worldwide globalization, the microbiota of populations maintaining traditional diets and lifestyles is a compelling topic for research [8]. For example, studies of populations in Burkina Faso, Tanzania, Mexico, and Venezuela showed a more diverse microbiota compared with industrialized Western populations [9–12]. Severe cold climates have fostered a distinct polar (northern) metabolism among indigenous peoples of the North. Based on the dietary predominance of proteins and lipids, this metabolism type directly addresses elevated energy requirements and thermogenic needs [13, 14]. Despite global transformations, traditional diet and lifestyle continue to occupy a substantial niche in the lives of indigenous peoples of the North. Formed in these conditions, the microbiota has distinct characteristics that differentiate it from that of other populations and exert influence on host health.
The study aimed to assess the factors and principles of microbiota formation in extreme climatic conditions and its possible role in health of indigenous peoples of the North based on a literature review.
MATERIALS AND METHODS
We conducted a systematic review of the literature using ScR methodology (scoping review) based on the PRISMA recommendations [15]. We searched for sources using keywords in the eLIBRARY.RU, PubMed, and Google Scholar databases. Keywords for sources included микробиота (microbiota) and Север (North) for Russian-language sources; gut microbiome, Arctic or gut microbiome, Inuit for the PubMed database in English; микробиота кишечника (gut microbiota), Север (North) for Google Scholar in Russian; and gut microbiome, 16S rRNA, indigenous people, Arctic in English. We independently reviewed the titles and abstracts of the publications for compliance with the inclusion criteria; any disagreements were resolved through negotiations. We also performed a manual search for additional sources in the reference lists of the articles we found.
The inclusion criteria were the following: 1) language: Russian, English; 2) study population: indigenous peoples of the North and the Arctic (the Inuit, the Yakuts, other indigenous peoples of the North); 3) age of participants over 18 years; 4) original studies of gut microbiota; 5) study method: 16S rRNA sequencing of bacteria. Exclusion criteria: studies of the gut microbiome of animals or children, review articles. The last search was conducted on April 22, 2024.
The initial screening using the above search queries yielded 13 publications from the eLIBRARY.RU database, 29 publications from the PubMed database using the Humans filter, 1,170 results for the Russian-language query, and 14,700 results for the English-language query from the Google Scholar database. After evaluating titles and abstracts, we excluded duplicates and publications that did not meet the inclusion criteria. After filtering, five sources remained. The stages of article selection are presented in Fig. 1.
Fig. 1. Flow-chart for selection of articles.
The taxonomy of microorganisms in the article is given in accordance with the latest version of the taxonomic database of the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi). Earlier versions of taxon names are given in brackets.
RESULTS
Studies to investigate the gut microbiota of indigenous peoples of the North are scarce; 16S rRNA data of Canadian Inuit, Alaska Natives, and the Yakuts were published (Table 1).
Table 1. Studies of gut microbiota in populations of indigenous peoples of the North
Northern population, n | Comparison population, n | Source |
Inuit of Canada, n=19 | Europeans of Montreal, n=26 | [16] |
Inuit of Canada, n=15 | Europeans of Montreal, n=9 | [17] |
Inuit of Canada, n=275 | Non-industrial, n=73 Industrial, n=104 | [18] |
Alaska natives, n=32 | Rural people of Africa, n=21 | [20] |
Yakuts, Russian Federation, n=11 (healthy) | Residents of Moscow, n=101 | [22] |
Girard et al. compared the gut microbiome of a small Canadian Arctic Inuit population and Caucasian individuals from Montreal, within Canada’s temperate climate zone [16]. The majority of Inuit adhered to a traditional Inuit diet and consumed arctic char, reindeer meat, marine mammals, or raw game every day, whereas the Caucasian individuals from Montreal adhered to a Western diet. In terms of taxon diversity and representation, the gut microbiota profile of Nunavut and Montreal residents was similar and close to other Western populations, while differing significantly from residents of Burkina Faso, Tanzania, and Venezuela with traditional lifestyles.
To identify Nunavut Inuit microbiota biomarkers, we used linear discriminant analysis, which showed the following taxa: representatives of the Bacillota (formerly Firmicutes) phylum, i.e. the Lachnospiraceae family, which ferment polysaccharides to form SCFAs, and the Peptococcus genus, which metabolizes peptone and amino acids to form fatty acids, synthesizing hydrogen sulfide, acetic, lactic, citric, isovaleric, and other acids; representatives of the Bacteroidota (formerly Bacteroidetes) phylum, i.e. the Bacteroidales order; poorly studied representatives of the Pseudomonadota (formerly Proteobacteria) phylum such as the Betaproteobacteria class and the Bilophila genus, which produce hydrogen sulfide from taurine; the Cyanobacteriota phylum. Lachnospiraceae, Betaproteobacteria, and Bilophila representatives were also identified as biomarkers for the Inuit diet. The authors identified differences between the two populations at the strain level. Representatives of the Prevotella genus (Bacteroidota phylum) were found in both Montreal and Nunavut samples; however, seven operational taxonomic units (OTUs) were associated with the Western diet, while only one was associated with the Inuit one. Differences in OTUs were also detected within the Akkermansia genus of the Verrucomicrobiota (formerly Verrucomicrobia) phylum, which was found in both populations.
A further study investigated changes in the gut microbiota of the Inuit from the same region of Canada over time during one year [17]. The taxonomic profile of the Inuit microbiota in this case differed from previous results. However, some taxa were consistent with those previously identified. In this study, the following were identified as markers of the Inuit microbiota: representatives of the Bacillota (formerly Firmicutes) phylum such as the Erysipelotrichales order, which is associated with lipid metabolism; the Megasphaera genera, which produce SCFAs; Eubacterium, Lactobacillus, Peptococcus with a wide range of metabolic functions; representatives of the Bacteroidota (formerly Bacteroidetes) phylum such as the Bacteroidales order and the Prevotella genus, which also produce SCFAs; representatives of the Actinomycetota (formerly Actinobacteria) phylum such as the Bifidobacteriaceae family, which produce lactate and support the intestinal barrier, the Coriobacteriales order, which converts bile salts and steroids in the intestine and activates dietary polyphenols; representatives of the Fusobacteriota (formerly Fusobacteria) phylum such as the Fusobacteriales order, which produce butyric acid, and others.
There were no obvious seasonal changes in the microbiomes of participants from Nunavut or Montreal. Intraindividual microbial diversity varied more in Nunavut residents than in Montreal residents, consistent with a more diverse and highly individualized diet in Nunavut. More diverse microbiomes tended to have a stable profile over time. The study found that traditional foods (raw fish, raw game meat, and fermented meat) influenced the microbiome profile in the Inuit. Based on the two studies, the authors noted that modifications towards a Western diet in the Inuit contributed to decreased microbiome diversity and seasonal variability [17].
The gut microbiota of the Inuit youth from Nunavik, another northern province of Canada, was investigated by Abed et al. [18]. The study participants also consumed traditional foods such as marine and land mammals, fish, shellfish, and wild birds and plants. These data were assessed in comparison with industrial and non-industrial populations selected from MetagenomicData R [19]. The Nunavik Inuit were found to have a homogeneous microbiome, as evidenced by low interindividual diversity but high intraindividual diversity.
The genomic microbiome content in the Nunavik Inuit was shown to be distinct from other previously studied populations, including that of the Nunavut Inuit. Although the Nunavik diet is rich in animal products, the predominant species in their microbiome were saccharolytic and produced SCFAs, mainly butyrate. Other metabolic products of the Inuit microbiome included acetate and propionate. Two species of bacteria, Ruminococcus bromii and Bifidobacterium adolescentis, used starch as an energy source and broke it down into acetate and lactate. The main metabolic pathways in the Inuit metagenomes included the biosynthesis of amino acids such as the synthesis of L-isoleucine from threonine, L-valine, precursors of phenylalanine, tryptophan, tyrosine, and folates. The authors suggested that protein fermentation (in the diet) may also significantly influence the gut microbiome profile of the Nunavik Inuit. Overall, taxonomic and functional features suggested that the Inuit gut microbiome was able to adapt to various factors and maintain host health. Although defining a healthy or robust microbiome is difficult, some characteristics of the Nunavik gut microbiome (such as high intraindividual diversity, dominance of SCFA-producing bacteria [primarily butyrate], and a potential capacity for resilience against environmental stress such as antibiotics) contribute to the maintenance of host homeostasis and improve health outcomes within the Arctic environment.
In 2020, a study was conducted to compare the gut microbiota of Alaska Natives with rural Africans in relation to the high risk of colorectal cancer in rural Africans [20]. Healthy Alaska Natives had lower intraindividual diversity (alpha diversity) of their microbiota compared with rural South Africans. Increased levels of Actinomycetota (formerly Actinobacteria) and Verrucomicrobiota (formerly Verrucomicrobia) were seen. The content of saccharolytic bacteria families such as Oscillospiraceae (formerly Ruminococcaceae) and Prevotellaceae was reduced, while the content of Lachnospiraceae (due to the Blautia and Lachnoclostridium genera) was increased. The Escherichia, Shigella, and Bifidobacterium genera were also common in the gut of Alaskans. Choline and formate were major intestinal metabolites in Alaska Natives, while Africans had more diverse metabolic pathways. Alaska Natives were shown to have high levels of 7-α-dehydroxylating bacteria, which are involved in bile acid metabolism and production of secondary bile acids, thus maintaining gut health and reducing the risk of metabolic disease [21].
As for indigenous peoples of the North of Russia, a study was conducted to investigate the gut microbiota of a small population of the Yakuts [22]. The Yakuts live in a vast territory of northeastern Russia in an extreme, sharply continental climate and, unlike the indigenous peoples of North America, are primarily pastoralists, raising cattle and horses. Hunting and fishing also play a significant role in their traditional way of life. The Yakut diet is based on various dairy products, meat of domestic and wild animals, and lake fish. A pilot study to evaluate the feces of 11 healthy representatives of the Yakuts showed that their gut microbiota differed from that of Moscow residents in terms of diversity and structure of taxonomic composition. Intraindividual diversity was statistically significantly higher in the Yakuts than in urban residents. An increased level of 11 genera and a decreased level of 9 genera of microorganisms were seen in the microbiota of the Yakuts. In the Yakut samples, Bacillota (formerly Firmicutes) was the predominant phylum (79%), and the ratio of Bacillota (Firmicutes) to Bacteroidota (Bacteroidetes) was 9.4 to 1.0. At the phylum level, a significant increase in the proportion of the Actinomycetota (formerly Actinobacteria) was found. Among representatives of Bacillota (formerly Firmicutes), an increased level of the Erysipelotrichales order was found, including the Coprobacillaceae family (in the Yakuts, Catenibacterium were found). They were associated with immunogenicity, but their role remains unclear. There were also producers of active cellulases such as bacteria of the Oscillospiraceae family (formerly Ruminococcaceae) and degraders of plant materials such as representatives of the Lachnospiraceae family (Blautia genus), which also actively ferment fats. The optimal balance of these bacteria regulate carbohydrate metabolism and reduce the risk of metabolic disease. Anaerobic conditions in the intestine are also maintained by facultative aerobic bacteria of the Bifidobacterium genus and the Coriobacteriaceae family, which belong to the Actinomycetota (formerly Actinobacteria) phylum; they absorb oxygen from the blood.
The microbiota of the Yakuts had some specific features. In particular, Ligilactobacillus ruminis (formerly Lactobacillus ruminis), an atypical representative of the Lactobacillaceae family with unique immunomodulatory and probiotic activity, was identified, which was not found in Moscow residents. L. ruminis suppressed pathogenic flora by producing lactic acid and reducing the pH values [23]. L. ruminis suppressed pathogenic flora by producing lactic acid and reducing the pH values. L. ruminis strains were shown to modulate immune response by decreasing levels of some proinflammatory cytokines and increasing levels of IL8 and NF-kB. L. ruminis was shown to significantly improve gut microbiota diversity in mice [24]. They produce lactase, thus alleviating lactose intolerance that can be genetically identified in the Yakuts [25].
Non-pathogenic Treponema succirifaciens was found in the Yakut microbiome. It is common in traditional rural populations and related to transmission from animals [26]. These bacteria have an enzyme called pyruvate formate lyase to oxidize pyruvate to acetyl-CoA and formate. This involves interactions with other commensal bacterial species that decompose plant fibers. T. succirifaciens is very sensitive to antibiotics and, therefore, cannot be found in the urban population. This suggests the beneficial influence of the traditional pastoral lifestyle on the microbiota of the modern indigenous peoples of Yakutia.
Microbiota diversity and profile in the indigenous peoples of the North are presented in Table 2.
Table 2. Microbiome of indigenous peoples of the North in comparison with other populations
Population | Microbiome diversity | Features | The most significant biomarkers (top 5) and their taxonomic affiliation: domain; type; class; order; family; genus | Source |
Inuit of Nunavut, Canada | No differences from Montreal Caucasian participants | Similar microbial profiles in the Inuit of Nunavut and residents of Montreal. Some poorly studied taxa found in the Inuit. Differences in species variety | – Bacteria; Bacillota; Clostridia; Lachnospirales; Lachnospiraceae; – Bacteria; Bacteroidota; Bacteroidia; Bacteroidales; Muribaculaceae; – Bacteria; Pseudomonadota; Betaproteobacteria; – Bacteria; Pseudomonadota; Betaproteobacteria; Burkholderiales; – Bacteria; Pseudomonadota; Betaproteobacteria; Burkholderiales; Sutterellaceae; Sutterella; | [16] |
Inuit of Nunavut, Canada | No differences from Montreal Caucasian participants | Traditional Inuit foods affecting microbiome profile | – Bacteria; Bacteroidota; Bacteroidia; Bacteroidales; Muribaculaceae; – Bacteria; Actinomycetota; Actinomycetes; Bifidobacteriales; Bifidobacteriaceae; – Bacteria; Bacillota; Bacilli; – Bacteria; Bacillota; Negativicutes; Veillonellales; Veillonellaceae; Megasphaera; – Bacteria; Bacteroidota; Bacteroidia; Bacteroidales; Prevotellaceae; Prevotella | [17] |
Inuit of Nunavik (Quebec), Canada | Intraindividual diversity of the Nunavik gut microbiome was significantly higher than in non-industrial and industrial populations | The Inuit microbiome differed from other industrial and non-industrial populations. SCFA-producing bacteria predominating in microbiome structure | – Bacteria; Actinomycetota; Coriobacteriia; Coriobacteriales; Coriobacteriaceae; Enorma; – Bacteria; Bacteroidota; Bacteroidia; Bacteroidales; Prevotellaceae; Prevotella; – Bacteria; Bacillota; Erysipelotrichia; Erysipelotrichales; Erysipelotrichaceae; [Clostridium] innocuum; – Bacteria; Bacillota; Clostridia; Eubacteriales; Oscillospiraceae; Flavonifractor; – Bacteria; Bacillota; Clostridia; Lachnospirales; Lachnospiraceae; Enterocloster | [18] |
Alaska Natives | Lower diversity in Alaska Natives vs rural Africans | Increased levels of Actinomycetota (formerly Actinobacteria) and Verrucomicrobiota (formerly Verrucomicrobia). Low levels of saccharolytic bacteria and higher microbial capacity for converting bile acids | – Bacteria; Bacillota; Clostridia; Lachnospirales; Lachnospiraceae; – Bacteria; Bacillota; Clostridia; Lachnospirales; Lachnospiraceae; Blautia; – Bacteria; Bacillota; Clostridia; Lachnospirales; Lachnospiraceae; Lachnoclostridium; – Bacteria; Actinomycetota; Actinomycetes; Bifidobacteriales; Bifidobacteriaceae; Bifidobacterium; – Bacteria; Pseudomonadota; Gammaproteobacteria; Enterobacterales; Enterobacteriaceae; Escherichia-Shigella | [20] |
Yakuts of the Russian Federation | Intraindividual diversity of the microbiome in healthy Yakuts higher than in Moscow residents | The microbiota of the Yakuts differs from that of the Inuit and residents of central Russia. High Bacillota (Firmicutes) to Bacteroidota (Bacteroidetes) ratio. Increased levels of Actinomycetota (formerly Actinobacteria) phylum | – Bacteria; Bacillota; Erysipelotrichia; Erysipelotrichales; Coprobacillaceae; Catenibacterium; – Bacteria; Bacillota; Bacilli; Lactobacillales; Lactobacillaceae; Lactobacillus; – Bacteria; Actinomycetota; Coriobacteriia; Coriobacteriales; Coriobacteriaceae; – Bacteria; Bacillota; Clostridia; Eubacteriales; Oscillospiraceae; Ruminococcus; – Bacteria; Bacillota; Clostridia; Lachnospirales; Lachnospiraceae | [22] |
DISCUSSION
Microbiota under cold stress conditions
The ecological niche of residence and biotic interactions with the environment have an obvious modulating effect on the gut microbiota profile. Under cold exposure, metabolic pathways are remodulated to maintain thermogenesis, where gut microbiota plays an important role. The review showed that the gut microbiota of the populations of the North has not been well studied. However, in recent years, animal studies allowed understanding the principles of interactions between the microbiota and the host organism during cold stress [27–29]. Chevalier et al. [27] showed that cold exposure in mice to develop cold tolerance led to changes in the microbiota taxonomic profile, increasing Firmicutes (formerly Firmicutes) vs Bacteroidota (formerly Bacteroidetes) ratio and almost completely depleting the Akkermansia genus, a representative of the Verrucomicrobiota (formerly Verrucomicrobia) phylum [27]. Increased levels of the Bacillota (formerly Firmicutes) phylum due to the Bacteroidota (formerly Bacteroidetes) with cold exposure were also shown in other studies in rodents [28, 29]. The involvement of microbiota in cold adaptation was also confirmed by experiments on transplantation of microbiota from cold-adapted mice (called “cold microbiota”), which promoted cold tolerance in control mice [27, 29].
The cold microbiota enhances the production and consumption of thermal energy through several mechanisms. Firstly, with prolonged cold exposure and transplantation of cold microbiota, the absorption surface of the epithelial layer of the small intestine increased due to physiological gut elongation and villi thickening and elongation [27, 29]. Expanded gut volume and absorptive interface facilitated increased retention of undigested organic compounds. Following microbial fermentation, these compounds generate metabolites required for synthesis of energy storage molecules (fat) as an energy reservoir. Secondly, there is a competition for the consumption of energy substrates between microorganisms and host tissues. During adaptation to cold, the host eliminates bacteria that actively consume energy resources such as SCFAs, which can provide 5–10% of a person’s energy needs [30]. Elimination of G. Akkermansia as an active energy consumer can serve as an example. This enhances mobilization of energy resources to ensure thermogenesis during the development of cold tolerance in mice. Thirdly, when the metagenomic reads of the microbiota from cold-exposed mice were mapped to a gut microbial gene catalogue, the gut microbiota was shown to assist the host in resisting extreme temperatures through regulating the host’s insulin pathway [29]. During adaptation of mice to cold, the microbiota promoted a shift of the brown adipose tissue phenotype to the white adipose tissue with increased generation of thermal energy [31–34]. Other aspects that regulate host energetics and thermogenesis during cold acclimation include the interaction between the microbiota, gut, and brain, which is mediated through the biosynthesis of neurotransmitters [28]. SCFAs can also be signaling molecules by acting on receptors responsible for appetite regulation, thermoregulation, and energy homeostasis [35]. Adaptation of humans to prolonged cold exposure in the North is likely to be also associated with biochemical and physiological responses associated with taxonomic changes in the microbiota profile. They may determine the specific phenotype of indigenous peoples of the North.
Effects of the diet and lifestyle on the microbiota in the North
Besides climatic conditions, the human gut microbiota is also influenced by several key factors such as nutrition and lifestyle. This can be clearly seen in ethnic groups that live in comparably similar natural and climatic conditions in the North. In the Yakuts, the taxonomic profile of the microbiota in the large intestine has been formed by the traditional way of life of livestock breeders, who use herbivores such as cattle (cows) and horses as their main source of food. The modern diet of the Yakuts contains a lot of simple carbohydrates. Bacillota (formerly Firmicutes), the predominant phylum in the Yakut microbiome, had the most diverse profile of microorganisms with the gram-positive cell wall and an ability to ferment both cellulose and complex non-starch polysaccharides. Substrate specificity and differences in fermentation products depend on the genus and species of microorganisms. Bacteria of the Ruminococcaceae family, which were common in the test population of the Yakuts, are known to break down plant cellulose and anaerobically ferment glucose mainly to acetate but also to propionate and butyrate. The Lachnospiraceae, another common family, which includes the Blautia and Dorea genera, also metabolizes glucose and other carbohydrates but does not produce butyrate. Catenibacterium, a member of the Coprobacillaceae family, showed an association with a high consumption of fermented milk products, carbohydrates, and fiber in Tibetan highlanders [36]. Levels of this bacteria were shown to increase in people with obesity or those who consume animal fats. Other authors found a positive correlation between Catenibacterium and Ligilactobacillus ruminis (formerly Lactobacillus ruminis) and consumption of omega-6 fatty acids with food [37].
We can assume that the traditional Yakut diet, which is rich in carbohydrates and animal fats, is balanced by a microbiota shift towards increased Bacillota (formerly Firmicutes) levels. Indirectly supported by murine cold-exposure studies showing Bacillota proliferation, this shift can optimize energy balance in cold environments via enhanced caloric extraction. An increased ratio of Bacillota (Firmicutes) to Bacteroidota (Bacteroidetes) is considered to be associated with an increased risk of obesity. This association was explained by the lack of competition for energy sources produced by the microbiota between the microorganisms and the host [38]. However, the association of this parameter with obesity is considered debatable [39]. The concepts of the main enterotypes proposed by Wu et al. should probably also be updated [40].
Unlike the Yakuts, the life of the Inuit is connected with the sea, and their diet is based on marine carnivorous mammals, which can stay underwater for a long time and eat small marine animals, such as fish, mollusks, crustaceans, etc. Metabolic consequences of their underwater swimming include the accumulation of large amounts of glycogen in the muscles, which is used to generate energy by glycolysis during diving [41]. The Inuit diet, which is rich in protein and fat, results in increased levels of the Bacteroidota (formerly Bacteroidetes) phylum in the gut, making their microbiota closer to that of Western populations. In general, the gut microbiota of the northern populations increasingly resembles that of urbanized communities. This convergence is attributed to dietary transitions and the incorporation of industrially processed foods into the diets of the northern populations.
Microbiota in people in close contact with animals
These microbiome features may be associated with the microbial environment of the Inuit and the Yakuts, in particular their close contact with livestock or game animals.
The microbiota of the Inuit included high levels of anaerobic microorganisms such as Bacteroidota (formerly Bacteroidetes) and Pseudomonadota (formerly Proteobacteria) phyla. Seawater is a source of the Pseudomonadota (formerly Proteobacteria) phylum [42]. The Inuit eat marine carnivores that can stay underwater for long periods and feed on small marine animals. Most distal gut microbiome samples from many marine mammals, including herbivorous sirenians and carnivorous pinnipeds (seals, walruses, and sea lions), were predominantly composed of Bacteroidota (formerly Bacteroidetes), which can ferment starchy polysaccharides and proteins [43]. Here we can see some similarities in the gut microbiota profiles of humans and game animals.
Similarities in the gut microbiota profile were also found for the Yakuts and the rumen of ruminants (cattle). A significant proportion of the Yakut microbiome was taken by Bacillota (formerly Firmicutes), in particular bacteria of the Oscillospiraceae family (formerly Ruminococcaceae). They break down plant cellulose using glycoside hydrolases and are known as the basic component of the rumen microbiome in ruminants [44, 45].
Current evidence indicates that the gut microbiome of modern northern populations varies in diversity and taxonomic profiles. Besides climatic conditions, the taxonomic profile may be influenced by the diet and microbial exposure to domestic and wild animals. Further studies to investigate the microbiome of the populations of the North with different lifestyles and diets may help to identify the mechanisms underlying metabolic health in cold climates.
Conclusion
The role of gut microbiota in host health and adaptation to cold climate is undeniable. Based on animal experiments, the concept of cold microbiota was introduced: it has a high content of Bacillota (formerly Firmicutes) and promotes efficient thermogenesis through the synthesis of SCFAs, decreased consumption of energy substrates by bacteria, and regulation of the host insulin pathway. Cold microbiota is a promising area of research in terms of microbiota participation in maintaining host metabolism in the North.
A review of available studies on the 16S rRNA gut microbiome in populations of the North showed that their taxonomic profiles differed both from other populations and from each other. These studies are not sufficient to fully characterize the northern microbiota, but they can be used to draw some conclusions. Despite shared climatic conditions and dietary patterns, the populations of the North have variations in their traditional livelihoods, diets, and animal exposure, which is reflected in differences in their gut microbiota profiles.
The most adapted microbiome may form through the activation of different metabolic pathways under similar climatic conditions. In the Yakuts and the Inuit, gut microbiomes demonstrated high intraindividual diversity with a predominance of SCFA-producing bacteria. This profile confers metabolic advantages in cold environments through diverse metabolic functions and probiotic effects. Developing activities to preserve and reinforce these distinctive microbiome features in the populations of the North represents a critical priority for future research in this field.
Additional information
Authors’ contribution. T.M. Sivtseva — literature review, collection and analysis of literary sources, writing the text and editing the article; M.A. Stepanova — literature review, collection and analysis of literary sources, preparation and writing of the article; R.N. Zakharova — literature review, collection and analysis of literary sources, preparation and writing of the article; S.I. Semenov — literature review, collection and analysis of literary sources, preparation and writing of the article; V.L. Osakovsky — literature review, collection and analysis of literary sources, writing the text and editing the article. All authors confirm that their authorship meets the international ICMJE criteria (all authors have made a significant contribution to the development of the concept, research and preparation of the article, read and approved the final version before publication).
Funding source. This work was supported by the Ministry of Science and Higher Education of the Russian Federation (project FSRG-2023-0003).
Competing interests. The authors declare that they have no competing interests.
About the authors
Tatyana M. Sivtseva
North-Eastern Federal University named after M.K. Ammosov
Author for correspondence.
Email: tm.sivtseva@s-vfu.ru
ORCID iD: 0000-0002-1501-7433
SPIN-code: 9571-3044
Cand. Sci. (Biology)
Russian Federation, YakutskMichiye A. Stepanova
North-Eastern Federal University named after M.K. Ammosov
Email: michiyastepanov@gmail.com
Undergraduate Student
Russian Federation, YakutskRaisa N. Zakharova
North-Eastern Federal University named after M.K. Ammosov
Email: prn.inst@mail.ru
ORCID iD: 0000-0002-1395-8256
SPIN-code: 8399-6329
MD, Cand. Sci. (Medicine)
Russian Federation, YakutskSergey I. Semenov
North-Eastern Federal University named after M.K. Ammosov
Email: insemenov@yandex.ru
ORCID iD: 0000-0001-8099-2270
SPIN-code: 4442-3374
MD, Dr. Sci. (Medicine)
Russian Federation, YakutskVladimir L. Osakovsky
North-Eastern Federal University named after M.K. Ammosov
Email: iz_labgene@mail.ru
ORCID iD: 0000-0001-9529-2488
SPIN-code: 2730-0390
Cand. Sci. (Biology)
Russian Federation, YakutskReferences
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