Elevated rates of horizontal gene transfer in the industrialized human microbiome

Groussin, Mathieu; Sistiaga, Ainara; Kearney, Sean M.; Moniz, Katya; Noel, Mary; Hooker, Jeff; Gibbons, Sean M.; Ségurel, Laure; Froment, Alain; Said‐Mohamed, Rihlat; Fezeu, Alain; Juimo, Vanessa A.; Lafosse, Sophie; Tabe, Francis Ekwin; Girard, Catherine; Iqaluk, Deborah; Nguyen, Le Thanh Tu; Shapiro, Ben; Lehtimäki, Jenni; Ruokolainen, Lasse; Kettunen, Pinja; Vatanen, Tommi; Sigwazi, Shani; Mabulla, Audax; Domı́nguez-Rodrigo, Manuel; Nartey, Yvonne Ayerki; Agyei-Nkansah, Adwoa; Duah, Amoako; Awuku, Yaw Asante; Valles, Kenneth; Asibey, Shadrack Osei; Afihene, Mary; Roberts, Lewis R.; Plymoth, Amelie; Onyekwere, Charles; Summons, Roger E.; Xavier, Ramnik J.; Alm, Eric J.

doi:10.1016/j.cell.2021.02.052

Cited by 221 publications

(204 citation statements)

References 87 publications

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“…We assumed a recent (i.e. within the lifetime of the participant) intra-host transfer event if shared GA2 DNA regions are >99.99% identical [ 11 , 18 ]. Shared T6SS regions between two species indicated a single-species spread event, whereas we inferred multi-species spread if the identical region was found in at least three different species from the same community.…”

Section: Resultsmentioning

confidence: 99%

“…One caveat to note is that our MGE spread analysis was conducted using four datasets from industrialized lifestyles, largely from Bacteroides -dominated communities. Analyses of HGT events in Prevotella -dominated non-industrialized populations indicated less frequent HGT [ 18 ] and may show a different repertoire of MGEs and different frequency of multi-species spread.…”

Section: Resultsmentioning

confidence: 99%

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Mobile Type VI secretion system loci of the gut Bacteroidales display extensive intra-ecosystem transfer, multi-species spread and geographical clustering

2021

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The human gut microbiota is a dense microbial ecosystem with extensive opportunities for bacterial contact-dependent processes such as conjugation and Type VI secretion system (T6SS)-dependent antagonism. In the gut Bacteroidales, two distinct genetic architectures of T6SS loci, GA1 and GA2, are contained on Integrative and Conjugative Elements (ICE). Despite intense interest in the T6SSs of the gut Bacteroidales, there is only a superficial understanding of their evolutionary patterns, and of their dissemination among Bacteroidales species in human gut communities. Here, we combine extensive genomic and metagenomic analyses to better understand their ecological and evolutionary dynamics. We identify new genetic subtypes, document extensive intrapersonal transfer of these ICE to Bacteroidales species within human gut microbiomes, and most importantly, reveal frequent population fixation of these newly armed strains in multiple species within a person. We further show the distribution of each of the distinct T6SSs in human populations and show there is geographical clustering. We reveal that the GA1 T6SS ICE integrates at a minimal recombination site leading to their integration throughout genomes and their frequent interruption of genes, whereas the GA2 T6SS ICE integrate at one of three different tRNA genes. The exclusion of concurrent GA1 and GA2 T6SSs in individual strains is associated with intact T6SS loci and with an ICE-encoded gene. By performing a comprehensive analysis of mobile genetic elements (MGE) in co-resident Bacteroidales species in numerous human gut communities, we identify 74 MGE that transferred to multiple Bacteroidales species within individual gut microbiomes. We further show that only three other MGE demonstrate multi-species spread in human gut microbiomes to the degree demonstrated by the GA1 and GA2 ICE. These data underscore the ubiquity and dissemination of mobile T6SS loci within Bacteroidales communities and across human populations.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Mobile Type VI secretion system loci of the gut Bacteroidales display extensive intra-ecosystem transfer, multi-species spread and geographical clustering

2021

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“…These studies have largely concluded, although with some debate ( Andreani et al 2017 ; Shapiro 2017 ) that pangenomes are predominantly adaptive—that selection plays a bigger role in pangenome evolution than drift. Here we have refocused the study of pangenome evolution to shorter time scales that is within individual gut microbiomes in which gene transfer events likely occurred within a human lifespan ( Brito et al 2016 ; Groussin et al 2021 ). Based on microbiome data from a Fiji cohort, we found that mobile gene sequence evolution is more influenced by selective pressures at the level of gene function than at the human host level.…”

Section: Discussionmentioning

confidence: 99%

“…To fill this gap, we used a data set of 37,853 mobile genes involved in recent HGT events in the human gut ( Brito et al 2016 ). HGT is known to occur frequently within individual human gut microbiomes ( Smillie et al 2011 ; Yaffe and Relman 2020 ; Groussin et al 2021 ), making it an ideal system in which to study mobile gene evolution over short time scales. We mapped metagenomic reads from a cohort of 176 Fiji islander gut microbiomes to the set of mobile genes.…”

Section: Introductionmentioning

confidence: 99%

Mobile Gene Sequence Evolution within Individual Human Gut Microbiomes Is Better Explained by Gene-Specific Than Host-Specific Selective Pressures

N’Guessan

Brito

Serohijos

et al. 2021

Genome Biology and Evolution

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Pangenomes—the cumulative set of genes encoded by a population or species—arise from the interplay of horizontal gene transfer, drift, and selection. The balance of these forces in shaping pangenomes has been debated, and studies to date focused on ancient evolutionary time scales have suggested that pangenomes generally confer niche adaptation to their bacterial hosts. To shed light on pangenome evolution on shorter evolutionary time scales, we inferred the selective pressures acting on mobile genes within individual human microbiomes from 176 Fiji islanders. We mapped metagenomic sequence reads to a set of known mobile genes to identify single nucleotide variants (SNVs) and calculated population genetic metrics to infer deviations from a neutral evolutionary model. We found that mobile gene sequence evolution varied more by gene family than by human social attributes, such as household or village. Patterns of mobile gene sequence evolution could be qualitatively recapitulated with a simple evolutionary simulation without the need to invoke adaptive value of mobile genes to either bacterial or human hosts. These results stand in contrast with the apparent adaptive value of pangenomes over longer evolutionary time scales. In general, the most highly mobile genes (i.e. those present in more distinct bacterial host genomes) tend to have higher metagenomic read coverage and an excess of low-frequency SNVs, consistent with their rapid spread across multiple bacterial species in the gut. However, a subset of mobile genes– including those involved in defense mechanisms and secondary metabolism—showed a contrasting signature of intermediate-frequency SNVs, indicating species-specific selective pressures or negative frequency-dependent selection on these genes. Together, our evolutionary models and population genetic data show that gene-specific selective pressures predominate over human or bacterial host-specific pressures during the relatively short time scales of a human lifetime.

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“…The limited data that are available for these intermediate populations, such as individuals living in peri-urban towns in Peru and South Africa as well as an Irish indigenous group transitioning away from nomadic living, exhibit gut microbial signatures from both highly industrialized and traditional populations but also display features of their own ( 16 , 63 , 64 ). Similarly, a recent worldwide survey found gut microbial composition clustered by lifestyle, with urban nonindustrialized and rural industrialized falling between the more stereotypical urban industrialized and rural nonindustrialized populations ( 65 ). These intermediate microbial signatures are typically ascribed to lifestyle factors, and while human-animal interactions are not always explicitly measured, they may be reflected in the factors found to be significant.…”

Section: Variation In Human Microbial Communities Across Populationsmentioning

confidence: 97%

Variation in Microbial Exposure at the Human-Animal Interface and the Implications for Microbiome-Mediated Health Outcome

Kuthyar

Reese

2021

mSystems

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Elevated rates of horizontal gene transfer in the industrialized human microbiome

Cited by 221 publications

References 87 publications

Mobile Type VI secretion system loci of the gut Bacteroidales display extensive intra-ecosystem transfer, multi-species spread and geographical clustering

Mobile Type VI secretion system loci of the gut Bacteroidales display extensive intra-ecosystem transfer, multi-species spread and geographical clustering

Mobile Gene Sequence Evolution within Individual Human Gut Microbiomes Is Better Explained by Gene-Specific Than Host-Specific Selective Pressures

Variation in Microbial Exposure at the Human-Animal Interface and the Implications for Microbiome-Mediated Health Outcome

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