Human Salivary Amylase Gene Copy Number Impacts Oral and Gut Microbiomes

Poole, Angela C.; Goodrich, Julia K.; Youngblut, Nicholas D.; Luque, Guillermo G.; Ruaud, Albane; Sutter, Jessica L.; Waters, Jillian L.; Shi, Qiaojuan; El-Hadidi, Mohamed; Johnson, Lynn M.; Bar, Haim; Huson, Daniel H.; Booth, James G.; Ley, Ruth E.

doi:10.1016/j.chom.2019.03.001

Cited by 105 publications

(85 citation statements)

References 64 publications

(83 reference statements)

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“…Data from public databases. We constructed a metagenome sequence collection from (i) the newly generated data (above) to complement the 146 metagenomes previously reported by Poole et al in 2019 (53) and (ii) publicly available shotgun-metagenome sequences from stool samples included in the curatedMetagenomicData package of Bioconductor (54) for which BMI information was provided. For the latter, we restricted our analyses to individuals for which the following information was available: gender, age, country of origin, and BMI.…”

Section: Methodsmentioning

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

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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.

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Section: Methodsmentioning

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

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“…We generated 141 metagenomes from fecal samples obtained as part of a previous study (53) (Supplementary Table S2). Metagenomic libraries were prepared as described in Appendix 1, Additional methods.…”

Section: Methodsmentioning

confidence: 99%

“…We constructed a metagenome sequence collection from: i) the newly generated data (above) to complement the 146 metagenomes previously reported in Poole et al, 2019 (53); and ii) publicly available shotgun-metagenome sequences from stool samples included in the curatedMetagenomicData package of Bioconductor (54) for which BMI information was provided. For the latter, we restricted our analyses to individuals for which the following information was available: gender, age, country of origin, and BMI.…”

Section: Methodsmentioning

confidence: 99%

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

Ruaud¹,

Esquivel-Elizondo²,

J³

et al. 2019

Preprint

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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...

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“…The relative abundance of specific gut microbial members can be shaped by the host's genotype (Goodrich et al, 2016a). Research has shown that genome-wide markers have been associated with the beta diversity of the microbiome in humans (Ma et al, 2014;Blekhman et al, 2015), and variations in the copy number of the human salivary amylase gene AMY1 influences the diversity and function of the human oral and gut microbiome (Poole et al, 2019). Moreover, mouse knockout experiments identified genes involved in immunity, metabolism, and behavior that affect gut microbiota (Spor et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

The Gut Microbiota of Pheasant Lineages Reflects Their Host Genetic Variation

et al. 2020

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The host gut colonized enormous microbial community, which can be influenced by diet, diseases, behavior, age, gender, hereditary effects, and environmental factors. However, the relationship between gut microbiota and host genetic variation has not yet been elucidated. In this study, we chose five pheasant lineages-Ring-necked pheasant (RN), Manchurian pheasant (MX), Phasianus versicolor (PV), Shenhong pheasant (SP), and Melanistic mutant pheasant (MM)-to investigate the gut microbial composition of pheasants and its relationship with host genetic variation. Microbial classifications revealed 29 phyla and 241 genera presented in pheasants, with the dominant phylum of Firmicutes and the genus of Lactobacillus. Statistical analyses suggest that the relative abundance of 75 genera was significantly different among the five lineages. The most abundant genus carried by the RN and MM was Streptococcus, which was significantly lower in PV (p = 0.024). Conversely, Lactobacillus was the major genera in PV and MX. Moreover, the RN had the greatest microbial abundance, with a remarkably different microbial community than PV. The gut microbial diversity of PV was the lowest and diverged significantly from the RN and MX. Interestingly, the clustering of the MM and SP in the microbial dendrogram corresponded to their cluster in the host phylogeny. The host phylogenetic split of the RN, MX, and PV echoed their microbial distance. In conclusion, the congruence of host phylogeny and their gut microbial dendrograms implies that gut microbiota of pheasant lineages could reflect their host genetic variation.

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Human Salivary Amylase Gene Copy Number Impacts Oral and Gut Microbiomes

Cited by 105 publications

References 64 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

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

The Gut Microbiota of Pheasant Lineages Reflects Their Host Genetic Variation

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Human Salivary Amylase Gene Copy Number Impacts Oral and Gut Microbiomes

Cited by 105 publications

References 64 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

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

The Gut Microbiota of Pheasant Lineages Reflects Their Host Genetic Variation

Contact Info

Product

Resources

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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