Genomic diversity landscape of the honey bee gut microbiota

Ellegaard, Kirsten; Engel, Philipp

doi:10.1038/s41467-019-08303-0

Cited by 235 publications

(305 citation statements)

References 54 publications

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“…For example, multiple strains of a sulfur-oxidizing endosymbiont were found to co-colonize individual hosts of deep-sea mussels, presumably because they encode complementary functions [4, 5]. In contrast, strains of the human gut microbiota have been shown to segregate among individuals, resulting in host-specific genetic profiles [6–8]. However, despite the increased awareness of the existence and functional importance of strain-level diversity in host-associated bacterial communities, little is known about differences in diversity across host species, or the underlying mechanisms which constrain and maintain diversity within and among hosts.…”

Section: Introductionmentioning

confidence: 99%

“…Interestingly, previous studies on bacterial isolates have demonstrated an impressive amount of genomic diversity within phylotypes, where strains isolated from different hosts often represent divergent phylogenetic sub-lineages [14–17]. Moreover, a recent metagenomic analysis of the gut microbiota of the Western honey bee, Apis mellifera, found that even within the same host species divergent sub-lineages can be present [6]. We refer to these sub-lineages as sequence-discrete populations (SDPs), since metagenomic data demonstrated that they were discrete from each other [6], in addition to being sufficiently divergent to be considered as different bacterial species [18].…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, a recent metagenomic analysis of the gut microbiota of the Western honey bee, Apis mellifera, found that even within the same host species divergent sub-lineages can be present [6]. We refer to these sub-lineages as sequence-discrete populations (SDPs), since metagenomic data demonstrated that they were discrete from each other [6], in addition to being sufficiently divergent to be considered as different bacterial species [18]. Given these results, it is possible that bee species with similar phylotype-level composition in their gut microbiota harbor very different communities.…”

Section: Introductionmentioning

confidence: 99%

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Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species

Ellegaard¹,

Suenami

Miyazaki

et al. 2020

Preprint

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Most bacterial species encompass strains with vastly different gene content. Strain diversity in microbial communities is therefore considered to be of functional importance. Yet, little is known about the extent to which related microbial communities differ in diversity at this level and which underlying mechanisms may constrain and maintain strain-level diversity. Here, we used shotgun metagenomics to characterize and compare the gut microbiota of two honey bee species, Apis mellifera and Apis cerana, which have diverged about 6 mio years ago. While both host species are colonized by largely overlapping bacterial 16S rRNA phylotypes, we find that their communities are highly host-specific when analyzed with genomic resolution. Despite their similar ecology, A. mellifera displayed a much higher extent of strain-level diversity and functional gene content in the microbiota than A. cerana, per colony and per individual bee. In particular, the gene repertoire for polysaccharide degradation was massively expanded in the microbiota of A. mellifera relative to A. cerana. Bee management practices, divergent ecological adaptation, or habitat size may have contributed to the observed differences in microbiota composition of these two key pollinator species. Our results illustrate that the gut microbiota of closely related animal hosts can differ vastly in genomic diversity despite sharing similar levels of diversity at the 16S rRNA gene. This is likely to have consequences for gut microbiota functioning and host-symbiont interactions, highlighting the need for metagenomic studies to understand the ecology and evolution of microbial communities.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species

Ellegaard¹,

Suenami

Miyazaki

et al. 2020

Preprint

Self Cite

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“…microbiome of vertebrates (Schloissnig et al, 2013;Garud and Pollard, 2020) and invertebrates (Ellegaard and Engel, 2019), marine bacteria (Delmont et al, 2019;Salazar et al, 2019) or crustaceans (Madoui et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

metaVaR: introducing metavariant species models for reference-free metagenomic-based population genomics

Laso-Jadart

Ambroise

Peterlongo

et al. 2020

Preprint

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Motivation:The availability of large metagenomic data offers great opportunities for the population genomic analysis of uncultured organisms, especially for small eukaryotes that represent an important part of the unexplored biosphere while playing a key ecological role. However, the majority of these species lacks reference genome or transcriptome which constitutes a technical barrier for classical population genomic analyses. Results: We introduce the metavariant species (MVS) model, a representation of the species only by intra-species nucleotide polymorphism. We designed a method combining reference-free variant calling, multiple density-based clustering and maximum weighted independent set algorithms to cluster intraspecies variant into MVS directly from multisample metagenomic raw reads without reference genome or reads assembly. The frequencies of the MVS variants are then used to compute population genomic statistics such as FST in order to estimate genomic differentiation between populations and to identify loci under natural selection. The MVSs construction was tested on simulated and real metagenomic data. MVs showed the required quality for robust population genomics and allowed an accurate estimation of genomic differentiation (∆FST < 0.0001 and < 0.03 on simulated and real data respectively). Loci predicted under natural selection on real data were all found by MVSs. MVSs represent a new paradigm that may simplify and enhance holistic approaches for population genomics and evolution of microorganisms. Availability: The method was implemented in a R package, metaVaR. https://github.com/madoui/MetaVaR Contact: amadoui@genoscope.cns.fr

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“…Geographic isolation of individual hosts over the host life span would then lead to genetic isolation of the symbiont populations and to symbiont population structure. Genomic variation and genetic isolation have been observed for horizontally transmitted symbionts of the human gut microbiome 19 and of the honey bee gut microbiome 20 . Moreover, structured symbiont populations can also emerge within an individual host, as observed for Vibrio fischeri colonizing the squid light organ, where different light organ crypts are infected by a specific strain 21 .…”

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confidence: 99%

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

Picazo¹,

Ansorge

Petersen

et al. 2019

Preprint

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Eukaryotes are habitats for bacterial organisms where the host colonization and dispersal among individual hosts have consequences for the bacterial ecology and evolution. Vertical symbiont transmission leads to geographic isolation of the microbial population and consequently to genetic isolation of microbiotas from individual hosts. In contrast, the extent of geographic and genetic isolation of horizontally transmitted microbiota is poorly characterized.Here we show that chemosynthetic symbionts of individual Bathymodiolus brooksi mussels constitute genetically isolated populations. The reconstruction of core genome-wide strain sequences from high-resolution metagenomes revealed distinct phylogenetic clades. Nucleotide diversity and strain composition vary along the mussel lifespan and individual hosts show a high degree of genetic isolation. Our results suggest that the uptake of environmental bacteria is a restricted process in B. brooksi, where self-infection of the gill tissue results in serial founder effects during symbiont evolution. We conclude that bacterial colonization dynamics over the host life-cycle is thus an important determinant of population structure and genome evolution of horizontally transmitted symbionts.

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Genomic diversity landscape of the honey bee gut microbiota

Cited by 235 publications

References 54 publications

Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species

Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species

metaVaR: introducing metavariant species models for reference-free metagenomic-based population genomics

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

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