Bacterial Epigenomics: Coming of Age

Oliveira, Pedro H.

doi:10.1128/msystems.00747-21

Cited by 7 publications

(8 citation statements)

References 34 publications

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“…We also identify epigenetic diversity and microbiome differentiation that are independent of host heterozygosity or genetic differentiation but associated with each other. We cannot ascertain whether this association is due to the production of microbial metabolites regulating the epigenome (as in mammals 20 , 21 ), to the influence of the host epigenome on the microbiome, or co-variation in response to environmental pressures 71 . Yet, irrespective of its origin, the proportion of epigenetic and microbiome diversity unrelated to host genetics could provide an additional source of variation, potentially very important for fish with low genetic diversity.…”

Section: Discussionmentioning

confidence: 99%

“…In mammals, the host-gut microbiome interaction seems to be primarily mediated by microbiota-produced metabolites, such as short chain fatty acids (SCFAs), that modify the epigenome of gastrointestinal host cells through DNA methylation and histone acetylation, thereby altering the host cells’ function 20 . Thus, changes in the microbiota composition or diversity can alter the production of metabolites that regulate host DNA and histone modifications 21 . Microbiome composition and function are influenced by the environment and by intrinsic host factors such as age, sex, immunocompetence and genotype, although their relative influence varies 22 .…”

Section: Introductionmentioning

confidence: 99%

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Microbiome and epigenetic variation in wild fish with low genetic diversity

Anka,

Uren Webster,

Berbel-Filho

et al. 2024

Nat Commun

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Non-genetic sources of phenotypic variation, such as the epigenome and the microbiome, could be important contributors to adaptive variation for species with low genetic diversity. However, little is known about the complex interaction between these factors and the genetic diversity of the host, particularly in wild populations. Here, we examine the skin microbiome composition of two closely-related mangrove killifish species with different mating systems (self-fertilising and outcrossing) under sympatric and allopatric conditions. This allows us to partition the influence of the genotype and the environment on their microbiome and (previously described) epigenetic profiles. We find the diversity and community composition of the skin microbiome are strongly shaped by the environment and, to a lesser extent, by species-specific influences. Heterozygosity and microbiome alpha diversity, but not epigenetic variation, are associated with the fluctuating asymmetry of traits related to performance (vision) and behaviour (aggression). Our study identifies that a proportion of the epigenetic diversity and microbiome differentiation is unrelated to genetic variation, and we find evidence for an associative relationship between microbiome and epigenetic diversity in these wild populations. This suggests that both mechanisms could potentially contribute to variation in species with low genetic diversity.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Microbiome and epigenetic variation in wild fish with low genetic diversity

Anka,

Uren Webster,

Berbel-Filho

et al. 2024

Nat Commun

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“…In mammals, the host-gut microbiome interaction seems to be primarily mediated by microbiota-produced metabolites, such as short chain fatty acids (SCFAs), that modify the epigenome of gastrointestinal host cells through DNA methylation and histone acetylation, consequently altering the host cells' function 21 . Thus, changes in the microbiota composition or diversity can alter the production of metabolites that regulate the host DNA and histone modi cations 22 .…”

Section: Introductionmentioning

confidence: 99%

The interaction between microbiome and epigenetic diversity as a source of phenotypic variation for fish with low genetic diversity

Anka,

Webster,

Berbel-Filho

et al. 2023

Preprint

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Non-genetic sources of phenotypic variation, such as the epigenome and the microbiome, could be important sources of adaptive variation for species with low genetic diversity, but little is known about the complex interaction between them and the genetic diversity of the host, particularly in wild populations. We examined the skin microbiome composition of two closely related mangrove killifish species with different mating systems (self-fertilising and outcrossing) under sympatric and allopatric conditions, to partition the influence of the genotype and the environment on their microbiome and epigenetic profiles. The diversity and community composition of the skin microbiome were shaped by strong genotype by environment interactions. We also found positive relationships between individual genetic diversity (heterozygosity) and microbiome alpha diversity (Faith and Chao1 measures) and between epigenetic variation and alpha diversity (Simpson evenness). Individual pairwise epigenetic and microbiome differentiation were positively correlated and influenced by species. We propose that the interaction between the host genotype, the microbiome and the epigenome can provide a plastic response to environmental variation, particularly relevant for individuals with low genetic diversity, and highlight the importance of considering the holobiont as the unit of selection to understand adaptation to environmental change.

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“…2016 ; Beaulaurier et al . 2019 ; Oliveira 2021 ). Methylation at these sites occurs via the action of DNA methyltransferases ( Casadesús and Low 2006 ; Jablonka and Raz 2009 ; Heard and Martienssen 2014 ), which are ubiquitous across bacteria ( Oliveira and Fang 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Growth condition-dependent differences in methylation imply transiently differentiated DNA methylation states in Escherichia coli

Breckell

Silander

2022

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DNA methylation in bacteria frequently serves as a simple immune system, allowing recognition of DNA from foreign sources, such as phages or selfish genetic elements. However, DNA methylation also affects other cell phenotypes in a heritable manner (i.e. epigenetically). While there are several examples of methylation affecting transcription in an epigenetic manner in highly localised contexts, it is not well established how frequently methylation serves a more general epigenetic function over larger genomic scales. To address this question, here we use Oxford Nanopore sequencing to profile DNA modification marks in three natural isolates of E. coli. We first identify the DNA sequence motifs targeted by the methyltransferases in each strain. We then quantify the frequency of methylation at each of these motifs across the entire genome in different growth conditions. We find that motifs in specific regions of the genome consistently exhibit high or low levels of methylation. Furthermore, we show that there are replicable and consistent differences in methylated regions across different growth conditions. This suggests that during growth, E. coli transiently differentiates into distinct methylation states that depend on the growth state, raising the possibility that measuring DNA methylation alone can be used to infer bacterial growth states without additional information such as transcriptome or proteome data. These results show the utility of using Oxford Nanopore sequencing as an economic means to infer DNA methylation status. They also provide new insights into the dynamics of methylation during bacterial growth, and provide evidence of differentiated cell states, a transient analogue to what is observed in the differentiation of cell types in multicellular organisms.

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Bacterial Epigenomics: Coming of Age

Cited by 7 publications

References 34 publications

Microbiome and epigenetic variation in wild fish with low genetic diversity

Microbiome and epigenetic variation in wild fish with low genetic diversity

The interaction between microbiome and epigenetic diversity as a source of phenotypic variation for fish with low genetic diversity

Growth condition-dependent differences in methylation imply transiently differentiated DNA methylation states in Escherichia coli

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