Interspecies electron transfer in syntrophic methanogenic consortia: From cultures to bioreactors

Shen, Liang; Zhao, Qingchuan; Wu, Xuee; Li, Xiangzhen; Li, Qingbiao; Wang, Yuanpeng

doi:10.1016/j.rser.2015.10.102

Cited by 156 publications

(80 citation statements)

References 105 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Interspecies metabolite transfer corresponds to the diffusion of a metabolite (e.g., H 2 ) from the producer (e.g., C. minuta) to the consumer (e.g., M. smithii). As described by Fick's law of diffusion, the flux of a metabolite between two microorganisms is directly proportional to the concentration gradient and inversely proportional to the distance, such that the closer the microorganisms are, the better the H 2 transfer (35,36). Thus, within the flocs, the H 2 interspecies transfer would be more efficient, to the benefit of M. smithii.…”

Section: Discussionmentioning

confidence: 99%

Syntrophy via Interspecies H ₂ Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Ruaud

Esquivel-Elizondo

Cuesta-Zuluaga

et al. 2020

mBio

View full text Add to dashboard Cite

Across human populations, 16S rRNA gene-based surveys of gut microbiomes have revealed that the bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae cooccur and are enriched in individuals with a lean, compared to an obese, body mass index (BMI). Whether these association patterns reflect interactions between metabolic partners, as well as whether these associations play a role in the lean host phenotype with which they associate, remains to be ascertained. Here, we validated previously reported cooccurrence patterns of the two families and their association with a lean BMI with a meta-analysis of 1,821 metagenomes derived from 10 independent studies. Furthermore, we report positive associations at the genus and species levels between Christensenella spp. and Methanobrevibacter smithii, the most abundant methanogen of the human gut. By coculturing three Christensenella spp. with M. smithii, we show that Christensenella spp. efficiently support the metabolism of M. smithii via H2 production far better than Bacteroides thetaiotaomicron does. Christensenella minuta forms flocs colonized by M. smithii even when H2 is in excess. In culture with C. minuta, H2 consumption by M. smithii shifts the metabolic output of C. minuta’s fermentation toward acetate rather than butyrate. Together, these results indicate that the widespread cooccurrence of these microorganisms is underpinned by both physical and metabolic interactions. Their combined metabolic activity may provide insights into their association with a lean host BMI. IMPORTANCE The human gut microbiome is made of trillions of microbial cells, most of which are Bacteria, with a subset of Archaea. The bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae are widespread in human guts. They correlate with each other and with a lean body type. Whether species of these two families interact and how they affect the body type are unanswered questions. Here, we show that species within these families correlate with each other across people. We also demonstrate that particular species of these two families grow together in dense flocs, wherein the bacteria provide hydrogen gas to the archaea, which then make methane. When the archaea are present, the ratio of bacterial products (which are nutrients for humans) is changed. These observations indicate that when these species grow together, their products have the potential to affect the physiology of their human host.

show abstract

Section: Discussionmentioning

confidence: 99%

Syntrophy via Interspecies H ₂ Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Ruaud

Esquivel-Elizondo

Cuesta-Zuluaga

et al. 2020

mBio

View full text Add to dashboard Cite

show abstract

“…Shewanella oneidensis produces outer membrane extensions (Pirbadian et al, 2014) that look very similar to the nanotubes of other bacteria. It is often stated that the S. oneidensis outer membrane extensions form electrical connections between cells (Benomar et al, 2015;Blumberger, 2015;Shen et al, 2015), presumably because the S. oneidensis outer membrane extensions are referred to as microbial nanowires (Pirbadian et al, 2014). However, as previously reviewed , there is no evidence that the S. oneidensis membrane extensions facilitate cell-to-cell electron transfer or any other form of long-range electron transport under physiologically relevant conditions.…”

Section: Biological Nanotubes and Related Cell-tocell Connectionsmentioning

confidence: 99%

Happy together: microbial communities that hook up to swap electrons

2016

View full text Add to dashboard Cite

The discovery of direct interspecies electron transfer (DIET) and cable bacteria has demonstrated that microbial cells can exchange electrons over long distances (μm-cm) through electrical connections. For example, in the presence of cable bacteria electrons are rapidly transported over centimeter distances, coupling the oxidation of reduced sulfur compounds in anoxic sediments to oxygen reduction in overlying surficial sediments. Bacteria and archaea wired for DIET are found in anaerobic methane-producing and methane-consuming communities. Electrical connections between gut microbes and host cells have also been proposed. Iterative environmental and defined culture studies on methanogenic communities revealed the importance of electrically conductive pili and c-type cytochromes in natural electrical grids, and demonstrated that conductive carbon materials and magnetite can substitute for these biological connectors to facilitate DIET. This understanding has led to strategies to enhance and stabilize anaerobic digestion. Key unknowns warranting further investigation include elucidation of the archaeal electrical connections facilitating DIET-based methane production and consumption; and the mechanisms for long-range electron transfer through cable bacteria. A better understanding of mechanisms for cell-to-cell electron transfer could facilitate the hunt for additional electrically connected microbial communities with omics approaches and could advance spin-off applications such as the development of sustainable bioelectronics materials and bioelectrochemical technologies.

show abstract

“…g ., M. smithii ). As described by Fick’s law of diffusion, the flux of a metabolite between two microorganisms is directly proportional to the concentration gradient and inversely proportional to the distance, such that the closer the microorganisms are, the better the H 2 transfer (35, 36). Thus, within the flocs the H 2 interspecies transfer would be more efficient, to the benefit of M. smithii .…”

Section: Discussionmentioning

confidence: 99%

Syntrophy via interspecies H₂transfer betweenChristensenellaandMethanobrevibacterunderlies their global co-occurrence in the human gut

Ruaud¹,

Esquivel-Elizondo²,

J³

et al. 2019

Preprint

View full text Add to dashboard Cite

23Across human populations, 16S rRNA gene-based surveys of gut microbiomes 24 have revealed that the bacterial family Christensenellaceae and the archaeal family 25Methanobacteriaceae co-occur and are enriched in individuals with a lean, compared to 26 an obese, BMI. Whether these association patterns reflect interactions between 27 metabolic partners remains to be ascertained, as well as whether these associations 28 play a role in the lean host phenotype with which they associate. Here, we validated 29 previously reported co-occurrence patterns of the two families, and their association 30 with a lean BMI, with a meta-analysis of 1,821 metagenomes derived from 10 31 independent studies. Furthermore, we report positive associations at the genus and 32 species level between Christensenella spp. and Methanobrevibacter smithii, the most 33 abundant methanogen of the human gut. By co-culturing three Christensenella spp. with 34 M. smithii, we show that Christensenella spp. efficiently support the metabolism of M. 35 smithii via H 2 production, far better than Bacteroides thetaiotaomicron. C. minuta forms 36 flocs colonized by M. smithii even when H 2 is in excess. In culture with C. minuta, H 2 37 consumption by M. smithii shifts the metabolic output of C. minuta's fermentation 38 towards acetate rather than butyrate. Together, these results indicate that the 39 widespread co-occurrence of these microbiota is underpinned by both physical and 40 metabolic interactions. Their combined metabolic activity may provide insights into their 41 association with a lean host BMI. 42 43 44 45 Importance 46 The human gut microbiome is made of trillions of microbial cells, most of which 47 are Bacteria, with a subset of Archaea. The bacterial family Christensenellaceae and 48 the archaeal family Methanobacteriaceae are widespread in human guts. They correlate 49with each other and with a lean body type. Whether species of these two families 50 interact, and how they affect the body type, are unanswered questions. Here, we 51 showed that species within these families correlate with each other across people. We 52 also demonstrated that particular species of these two families grow together in dense 53 flocs, wherein the bacteria provide hydrogen gas to the archaea, which then make 54 methane. When the archaea are present, the ratio of bacterial products (which are 55 nutrients for humans) is changed. These observations indicate when these species 56 grow together, their products have the potential to affect the physiology of their human 57 host. 58 the human gut microbiome, the family Christensenellaceae was described relatively 65 recently, when the type strain Christensenella minuta was reported in 2012 (16). Prior to 66 the description of C. minuta, 16S rRNA sequences from this genus escaped notice in 67 the gut microbiome, though these sequences accumulated steadily in SSU rRNA gene 68 databases. A positive association between a lean host BMI and the relative abundance 69 in the gut of Christensenellaceae 16S rRNA genes was fi...

show abstract

Interspecies electron transfer in syntrophic methanogenic consortia: From cultures to bioreactors

Cited by 156 publications

References 105 publications

Syntrophy via Interspecies H ₂ Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Syntrophy via Interspecies H ₂ Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Happy together: microbial communities that hook up to swap electrons

Syntrophy via interspecies H₂transfer betweenChristensenellaandMethanobrevibacterunderlies their global co-occurrence in the human gut

Contact Info

Product

Resources

About

Interspecies electron transfer in syntrophic methanogenic consortia: From cultures to bioreactors

Cited by 156 publications

References 105 publications

Syntrophy via Interspecies H 2 Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Syntrophy via Interspecies H 2 Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Happy together: microbial communities that hook up to swap electrons

Syntrophy via interspecies H2transfer betweenChristensenellaandMethanobrevibacterunderlies their global co-occurrence in the human gut

Contact Info

Product

Resources

About

Syntrophy via Interspecies H ₂ Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Syntrophy via Interspecies H ₂ Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut

Syntrophy via interspecies H₂transfer betweenChristensenellaandMethanobrevibacterunderlies their global co-occurrence in the human gut