Back to Search Start Over

Role of archaea in human disease

Authors :
Rustam Aminov
Source :
Frontiers in Cellular and Infection Microbiology, Vol 3 (2013), Frontiers in Cellular and Infection Microbiology
Publication Year :
2013
Publisher :
Frontiers Media S.A., 2013.

Abstract

A decade ago a hypothesis was proposed that, similar to the Bacteria and Eukarya, the archaeal domain of life might harbor certain species capable of causing disease (Cavicchioli et al., 2003; Eckburg et al., 2003). Now, a decade later, it is time to revisit the topic in the light of new data available. The last decade witnessed a massive use of molecular ecology tools in clinical microbiology, and these data can be inspected for the potential involvement of the Archaea in various infectious diseases in humans and animals. Unlike the Bacteria, the diversity of the Archaea in the human body is substantially lower, including representatives of only one phylum, Euryarchaeota. The phylum includes three species: Methanobrevibacter smithii, found mostly in the gut and vagina (Miller and Wolin, 1982; Belay et al., 1990); Methanosphaera stadtmanae, found mostly in the gut (Miller and Wolin, 1985); and M. oralis, found mostly in the oral cavity (Belay et al., 1988; Ferrari et al., 1994). Compared to bacteria, the relative abundance of archaea is also much lower (Miller and Wolin, 1982), although the recent improvements in cultivation and DNA detection may help to estimate these numbers more accurately (Dridi et al., 2009; Khelaifia et al., 2013). The first work suggesting an association of the Archaea with human gastrointestinal disease was published in 1985 (McKay et al., 1985). Patients with Crohn’s disease, ulcerative colitis and primary pneumatosis intestinalis displayed a significantly lower incidence of methane excretion compared to healthy subjects. On the contrary, patients with diverticulosis showed a significantly increased incidence of methanogens compared to control (Weaver et al., 1986). Since then, there have been a number of studies, with more recent ones using molecular ecology markers, such as the 16S rRNA and mcrA genes, which have confirmed these two initial observations. That is, in conditions characterized by extended transit time in the intestine, the incidence, and rate of methane production are higher (Fiedorek et al., 1990; Pimentel et al., 2003; Chatterjee et al., 2007), while the diarrheal conditions of human gastrointestinal disease result in the opposite trend with lower incidences of methanogenic archaea and lower rates of methane production (McKay et al., 1985; Scanlan et al., 2008). Chemotherapy-induced diarrhea in cancer patients has also resulted in the decrease of methanogenic archaea in parallel with the loss of beneficial bacteria (Stringer et al., 2013). Indeed, experimental interventions to increase the intestinal transit rate have resulted in the decline of fecal methanogens and methane production, while the opposite effect has been observed in the loperamide treatment group (Lewis and Cochrane, 2007). Recent reassessments of the role of methane production among patients with gastrointestinal disturbances have clearly associated elevated methane production with alterations in intestinal motility, such as constipation, but not with other conditions (Attaluri et al., 2010; Furnari et al., 2012). Thus, a pathogenic link with methanogens is unlikely (Di Stefano and Corazza, 2010), and their involvement in gastrointestinal disease is presently uncorroborated. From the ecological/system biology viewpoint the numbers and the methane production by archaea is more likely a reflection of syntrophic relationships in the gut where the local environment, depending on a number of factors, may favor hydrogen channeling through alternative mechanisms of hydrogen disposal, such as methanogenesis, sulfate reduction, or acetogenesis. In this regard, alternative generation of highly toxic hydrogen sulfide as a result of sulfate reduction in the gut may impose much higher health risks (Medani et al., 2011; Carbonero et al., 2012) compared to more inert methane. The best-studied cases of a potential involvement of the Archaea in human pathology, however, are linked to periodontal disease. Methanobrevibacter oralislike phylotypes, for example, have been detected by PCR in up to 36% of periodontitis patients (Lepp et al., 2004). In another study, five cases of apical periodontitis out of 20 total have been found positive for the Archaea (Vianna et al., 2006). The follow up work by the same group has greatly contributed to our understanding of the role played by hydrogenotrophic microorganisms in periodontal disease (Vianna et al., 2008). Compared to periodontitis patients, the supragingival plaque of healthy subjects harbors a lower total microbial load, and the hydrogenotrophic group is represented exclusively by acetogenic bacteria, also at lower numbers. On the contrary, the subgingival plaque from periodontitis patients harbors a larger number of total bacteria, and the hydrogenotrophic group includes methanogenic archaea and sulphate-reducing bacteria (SRB) in addition to acetogenic bacteria. The latter two groups are absent in healthy control subjects but present in 65% of periodontitis patients, alone or in combination (Vianna et al., 2008). It needs to be noted here that the presence of SRB in human saliva can be detected in 30% of subjects and, among other oral and systemic conditions, the only statistically significant association of the SRB carriage is with periodontitis (Heggendorn et al., 2013). Although the proportion of hydrogenotrophs in periodontal disease is below 1% of the total microbiota (Vianna et al., 2008), the hydrogen sink they provide may

Details

Language :
English
ISSN :
22352988
Volume :
3
Database :
OpenAIRE
Journal :
Frontiers in Cellular and Infection Microbiology
Accession number :
edsair.doi.dedup.....fd57016527668c7fedfe5bee6fb18b9b
Full Text :
https://doi.org/10.3389/fcimb.2013.00042