Abstract
The gut microbiota represents a complex and diverse ecosystem with a profound impact on human health, promoting immune maturation, and host metabolism as well as colonization resistance. Important members that have often been disregarded are the methanogenic archaea. Methanogenic archaea reduce hydrogen levels via the production of methane, thereby stimulating food fermentation by saccharolytic bacteria. On the other hand, colonization by archaea has been suggested to promote a number of gastrointestinal and metabolic diseases such as colorectal cancer, inflammatory bowel disease, and obesity. Archaea have been shown to be absent during infancy while omnipresent in school-aged children, suggesting that colonization may result from environmental exposure during childhood. The factors that determine the acquisition of methanogenic archaea, however, have remained undefined. Therefore, we aimed to explore determinants associated with the acquisition of the two main gastrointestinal archaeal species, Methanobrevibacter smithii and Methanosphaera stadtmanae, in children. Within the context of the KOALA Birth Cohort Study, fecal samples from 472 children aged 6–10 years were analyzed for the abundance of M. smithii and M. stadtmanae using qPCR. Environmental factors such as diet, lifestyle, hygiene, child rearing, and medication were recorded by repeated questionnaires. The relationship between these determinants and the presence and abundance of archaea was analyzed by logistic and linear regression respectively. Three hundred and sixty-nine out of the 472 children (78.2%) were colonized by M. smithii, and 39 out of the 472 children (8.3%) by M. stadtmanae. The consumption of organic yogurt (odds ratio: 4.25, CI95: 1.51; 11.95) and the consumption of organic milk (odds ratio: 5.58, CI95: 1.83; 17.01) were positively associated with the presence of M. smithii. We subsequently screened raw milk, processed milk, and yogurt samples for methanogens. We identified milk products as possible source for M. smithii, but not M. stadtmanae. In conclusion, M. smithii seems present in milk products and their consumption may determine archaeal gut colonization in children. For the first time, a large variety of determinants have been explored in association with gut colonization by methanogenic archaea. Although more information is needed to confirm and unravel the mechanisms in detail, it provides new insights on microbial colonization processes in early life.
Highlights
The human gut contains a complex and diverse ecosystem consisting of hundreds of microbial species that are acquired during the first years of life (van Best et al, 2015)
Five methanogenic archaea species and two halophilic archaea have been isolated from human feces from which only the Methanobrevibacter smithii (M. smithii), Methanosphaera stadtmanae (M. stadtmanae), and Methanomassiliicoccus luminyensis (M. luminyensis) have been detected more than once (Miller et al, 1982; Miller and Wolin, 1985; Dridi et al, 2012a; Khelaifia et al, 2013, 2017; Khelaifia and Raoult, 2016)
369 (78.2%) out of 472 were colonized by M. smithii, while 39 (8.3%) out of 472 children were colonized by M. stadtmanae
Summary
The human gut contains a complex and diverse ecosystem consisting of hundreds of microbial species that are acquired during the first years of life (van Best et al, 2015). A myriad of bacterial species have been studied within the human infant gut, important colonizers that are often disregarded are the methanogenic archaea (Horz, 2015). A previous study from Dridi et al showed that the most dominant archaeal gut inhabitant is M. smithii with a prevalence of 88% in children of 0–10 years of age. Methanogenic archaea are responsible for producing the majority of methane in the gut by reducing carbon dioxide into methane in the presence of hydrogen (Roccarina et al, 2010). Reduction of hydrogen levels by methanogens stimulates food fermentation by saccarolytic bacteria (Horz and Conrads, 2010; Gaci et al, 2014). In previous studies higher levels of archaea and excreted methane were found in patients with gastrointestinal and metabolic diseases such as colorectal cancer, inflammatory bowel disease, irritable bowel syndrome, constipation, and obesity (Haines et al, 1977; Pimentel et al, 2003; Kim et al, 2012; Blais Lecours et al, 2014; Triantafyllou et al, 2014; Mbakwa et al, 2015; Vandeputte et al, 2016)
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