Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life

Vatanen, Tommi; Plichta, Damian R.; Somani, Juhi; Münch, Philipp; Arthur, Timothy D.; Hall, Andrew Brantley; Rudolf, Sabine; Oakeley, Edward J.; Ke, Xiaobo; Young, Rachel; Haiser, Henry J.; Kolde, Raivo; Yassour, Moran; Luopajärvi, Kristiina; Siljander, Heli; Virtanen, Suvi Μ.; Ilonen, Jorma; Uibo, Raivo; Tillmann, Vallo; Mokurov, Sergei; Доршакова, Н. В.; Porter, Jeffrey A.; McHardy, Alice C.; Lähdesmäki, Harri; Vlamakis, Hera; Huttenhower, Curtis; Knip, Mikael; Xavier, Ramnik J.

doi:10.1038/s41564-018-0321-5

Cited by 189 publications

(190 citation statements)

References 74 publications

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“…Bifidobacterium bifidum, Bifidobacterium breve and Bifidobacterium longum, possess genetic adaptations to facilitate colonization of the infant gut (Matamoros et al, 2013;Milani et al, 2017b). Recently, a number of studies have presented comprehensive data showing that these three species can be maternally inherited by vertical transmission (Milani et al, 2015a;Duranti et al, 2017b;Vatanen et al, 2018;Moossavi et al, 2019). Further evidence has found that horizontal transfer of bifidobacterial DNA from mother to foetus may occur also via placenta (Satokari et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe‐host co‐evolution

Duranti

Lugli

Milani

et al. 2019

Environmental Microbiology

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Summary Bifidobacterium bifidum is reported to be among the first colonizers of the newborn's gastrointestinal tract due to its ability to metabolize human milk oligosaccharides (HMOs). In order to investigate biological features that allow this bifidobacterial species to colonize a newborn, bifidobacterial internally transcribed spacer profiling of stool samples of 50 mother‐infant dyads, as well as corresponding breastmilk samples, was performed. Hierarchical clustering based on bifidobacterial population profiles found in infant faecal samples revealed the presence of four bifidobacterial clusters or the so‐called bifidotypes. Bifidobacterium bifidum was shown to be a key member among bifidotypes, in which its presence correlate with several different bifidobacterial species retrieved in infant faecal samples. For this reason, we investigated cross‐feeding behaviour facilitated by B. bifidum on a bioreactor model using human milk as growth substrate. Transcriptional profiles of this strain were evaluated when grown on nine specific glycans typically constituting HMOs. Remarkably, these analyses suggest extensive co‐evolution with the host and other bifidobacterial species in terms of resource provision and sharing, respectively, activities that appear to support a bifidobacteria‐dominant microbiome.

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Section: Introductionmentioning

confidence: 99%

Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe‐host co‐evolution

Duranti

Lugli

Milani

et al. 2019

Environmental Microbiology

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“…Because it uses sample-assembled genomes and full paired-read information there is greatly increased confidence that reads are aligned correctly, which improves the high resolution comparisons being made based on entire genomes. Many of these capabilities have been successfully implemented individually in previous studies 15,19,[30][31][32][33] . However, their simultaneous integration into a well-documented and easy to use pipeline allows substantially more rigorous detection of near-identical strains than the existing commonly used pipelines ( Figure 2 ) used in recent high-profile publications to quantify the ecologically critical process of microbiome transmission 14,34 .…”

Section: Discussionmentioning

confidence: 99%

InStrain enables population genomic analysis from metagenomic data and rigorous detection of identical microbial strains

Olm

Crits-Christoph²,

Bouma‐Gregson³

et al. 2020

Preprint

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Coexisting microbial cells of the same species often exhibit genetic differences that can affect phenotypes ranging from nutrient preference to pathogenicity. Here we present inStrain, a program that utilizes metagenomic paired reads to profile intra-population genetic diversity (microdiversity) across whole genomes and compare populations in a microdiversity-aware manner, dramatically increasing genomic comparison accuracy when benchmarked against existing methods. We use inStrain to profile >1,000 fecal metagenomes from newborn premature infants and find that siblings share significantly more strains than unrelated infants, although identical twins share no more strains than fraternal siblings. Infants born via cesarean section harbored Klebsiella with significantly higher nucleotide diversity than infants delivered vaginally, potentially reflecting acquisition from hospital versus maternal microbiomes. Genomic loci showing diversity within an infant included variants found in other infants, possibly reflecting inoculation from diverse hospital-associated sources. InStrain can be applied to any metagenomic dataset for microdiversity analysis and rigorous strain comparison. MainCells in microbial populations are not all identical to one another. Genetic polymorphisms rapidly arise through de novo mutation, and these variants can spread because they confer a fitness advantage or by lateral gene transfer (if the variant confers an advantage or is linked to a fitness-conferring variant). It is estimated that billions to trillions of bacterial genetic mutations are generated de novo every day in the microbiome of an individual adult human 1 , and these differences can be clinically relevant. For example, just three point mutations can confer antibiotic resistance in Enterobacteriaceae 2 . Studying genetic variation in microbial populations has historically involved isolating a multitude of cells from the same population and performing phenotypic analysis and/or genome sequencing. Genome-resolved metagenomic analysis, which involves extracting and sequencing DNA directly from the environment and using computational tools to assemble and bin the resulting DNA sequences into genomes in silico , presents an attractive high-throughput alternative to this process. This technique allows simultaneous analysis of microbial communities, the species populations that comprise them, and heterogeneity within these populations, and has been used to reveal fine-scale evolutionary mechanisms 3-5 , dynamics 6-12 , and strain level metabolic variation that could contribute to strain selection 1,13 .Many fundamental questions in human microbiome research relate to the transmission of microbial populations between individuals, including how we are seeded by microbes early in life [14][15][16] . However, strain diversity presents challenges for such analyses. Sequence comparisons are usually performed by aligning consensus genomes assembled from different samples 1,17 or by modifying a reference genome using mapped reads and comparing it...

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“…[5,[22][23][24] Likewise, in adults, Firmicutes and Bacteroidetes are prominent in the gut, and metabolize dietary plant polysaccharides, which are otherwise indigestible by the mammalian host. Indeed, a mammalian host is unable to complete digestion of the entirety of food or to de novo produce all food-related vitamins that are critically important for a healthy living.…”

Section: Gut Microbes Are Essential For Food Digestionmentioning

confidence: 99%

When Cultures Meet: The Landscape of “Social” Interactions between the Host and Its Indigenous Microbes

2019

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Animals exist as biodiverse composite organisms that include microbial residents, eukaryotic cells, and organs that collectively form a human being. Through an interdependent relationship and an inherent ability to transmit and reciprocate stimuli in a bidirectional way, a human body or the holobiont secures growth, health, and reproduction. As such, the survival of a holobiont is dependent on the maintenance of biological order including metabolic homeostasis by tight regulation of the communication between its eukaryotic and prokaryotic residents. In this review an overview and perspective are provided on the bidirectional communication between microbes and their host in mutually nurturing biochemical, biological, and social interconnected relationships between the components of the holobiont. An emphasis is placed on exemplifying microbiome-mediated effects on host functions-aiming to integrate microbiome functionality to host physiology, be it health or disease. Nutrition, immunology, and sexual dimorphism have been traversed extensively to reflect on health and mind states, social interactions, and urbanization defects/effects. Finally, examples of molecular mechanisms potentially orchestrating these complex transkingdom interactions are provided. We Nurture an Intricate Relationship with Our Symbiotic MicrobesHumans and their indigenous microbiomes are uniquely symbiotic in a number of facets. Indeed, many human genes are homologous to bacterial genes that are predominant in

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Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life

Cited by 189 publications

References 74 publications

Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe‐host co‐evolution

Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe‐host co‐evolution

InStrain enables population genomic analysis from metagenomic data and rigorous detection of identical microbial strains

When Cultures Meet: The Landscape of “Social” Interactions between the Host and Its Indigenous Microbes

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