Horizontal gene transfer-mediated bacterial strain variation affects host fitness in Drosophila

Abstract Background How microbes affect host fitness and environmental adaptation has become a fundamental research question in evolutionary biology. To better understand the role of microbial genomic variation for host fitness, we tested for associations of bacterial genomic variation and Drosophila melanogaster offspring number in a microbial Genome Wide Association Study (GWAS). Results We performed a microbial GWAS, leveraging strain variation in the genus Gluconobacter, a genus of bacteria that are commonly associated with Drosophila under natural conditions. We pinpoint the thiamine biosynthesis pathway (TBP) as contributing to differences in fitness conferred to the fly host. While an effect of thiamine on fly development has been described, we show that strain variation in TBP between bacterial isolates from wild-caught D. melanogaster contributes to variation in offspring production by the host. By tracing the evolutionary history of TBP genes in Gluconobacter, we find that TBP genes were most likely lost and reacquired by horizontal gene transfer (HGT). Conclusion Our study emphasizes the importance of strain variation and highlights that HGT can add to microbiome flexibility and potentially to host adaptation.

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Horizontal gene transfer-mediated bacterial strain variation affects host fitness

10.1101/2020.09.24.311167 ◽

2020 ◽

Author(s):

Yun Wang ◽

Franz Baumdicker ◽

Sven Kuenzel ◽

Fabian Staubach

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary Biology ◽

Genome Wide Association Study ◽

Research Question ◽

Genomic Variation ◽

Strain Variation ◽

Host Fitness ◽

Offspring Number ◽

History Of

AbstractHow microbes affect host fitness and environmental adaptation has become a fundamental research question in evolutionary biology. We tested for associations of bacterial genomic variation and Drosophila melanogaster offspring number in a microbial Genome Wide Association Study (GWAS). Leveraging strain variation in the genus Gluconobacter, a genus of bacteria that are commonly associated with Drosophila under natural conditions, we pinpoint the thiamine biosynthesis pathway (TBP) as contributing to differences in fitness conferred to the fly host. By tracing the evolutionary history of TBP genes in Gluconobacter, we find that TBP genes were most likely lost and reacquired by horizontal gene transfer (HGT). We suggest that HGT might contribute to microbiome flexibility and speculate that it can also more generally contribute to host adaptation.

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A mobile genetic element increases bacterial host fitness by manipulating development

eLife ◽

10.7554/elife.65924 ◽

2021 ◽

Vol 10 ◽

Author(s):

Joshua M Jones ◽

Ilana Grinberg ◽

Avigdor Eldar ◽

Alan D Grossman

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Mobile Genetic Elements ◽

Selective Advantage ◽

Host Cells ◽

Bacterial Host ◽

Host Fitness ◽

Genetic Elements ◽

Necessary And Sufficient ◽

Integrative And Conjugative Element

Horizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial cargo genes. Uncovering strategies used by mobile genetic elements to benefit host cells is crucial for understanding their stability and spread in populations. We describe a benefit that ICEBs1, an integrative and conjugative element of Bacillus subtilis, provides to its host cells. Activation of ICEBs1 conferred a frequency-dependent selective advantage to host cells during two different developmental processes: biofilm formation and sporulation. These benefits were due to inhibition of biofilm-associated gene expression and delayed sporulation by ICEBs1-containing cells, enabling them to exploit their neighbors and grow more prior to development. A single ICEBs1 gene, devI (formerly ydcO), was both necessary and sufficient for inhibition of development. Manipulation of host developmental programs allows ICEBs1 to increase host fitness, thereby increasing propagation of the element.

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Experimental Evolution of Bacillus subtilis Reveals the Evolutionary Dynamics of Horizontal Gene Transfer and Suggests Adaptive and Neutral Effects

Genetics ◽

10.1534/genetics.120.303401 ◽

2020 ◽

Vol 216 (2) ◽

pp. 543-558

Author(s):

Shai Slomka ◽

Itamar Françoise ◽

Gil Hornung ◽

Omer Asraf ◽

Tammy Biniashvili ◽

...

Keyword(s):

Bacillus Subtilis ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary Dynamics ◽

De Novo ◽

Growth Yield ◽

Genomic Variation ◽

Bacterial Populations ◽

Flagellar Proteins ◽

Foreign Dna

Tracing evolutionary processes that lead to fixation of genomic variation in wild bacterial populations is a prime challenge in molecular evolution. In particular, the relative contribution of horizontal gene transfer (HGT) vs.de novo mutations during adaptation to a new environment is poorly understood. To gain a better understanding of the dynamics of HGT and its effect on adaptation, we subjected several populations of competent Bacillus subtilis to a serial dilution evolution on a high-salt-containing medium, either with or without foreign DNA from diverse pre-adapted or naturally salt tolerant species. Following 504 generations of evolution, all populations improved growth yield on the medium. Sequencing of evolved populations revealed extensive acquisition of foreign DNA from close Bacillus donors but not from more remote donors. HGT occurred in bursts, whereby a single bacterial cell appears to have acquired dozens of fragments at once. In the largest burst, close to 2% of the genome has been replaced by HGT. Acquired segments tend to be clustered in integration hotspots. Other than HGT, genomes also acquired spontaneous mutations. Many of these mutations occurred within, and seem to alter, the sequence of flagellar proteins. Finally, we show that, while some HGT fragments could be neutral, others are adaptive and accelerate evolution.

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The Enterococcus Cassette Chromosome, a Genomic Variation Enabler in Enterococci

mSphere ◽

10.1128/msphere.00402-18 ◽

2018 ◽

Vol 3 (6) ◽

Cited By ~ 1

Author(s):

A. Sivertsen ◽

J. Janice ◽

T. Pedersen ◽

T. M. Wagner ◽

J. Hegstad ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Enterococcus Faecium ◽

Genomic Variation ◽

Conjugative Plasmid ◽

Natural Habitats ◽

Chloramphenicol Resistance ◽

Content Type ◽

Serine Recombinases ◽

Accessory Genes

ABSTRACT Enterococcus faecium has a highly variable genome prone to recombination and horizontal gene transfer. Here, we have identified a novel genetic island with an insertion locus and mobilization genes similar to those of staphylococcus cassette chromosome elements SCCmec. This novel element termed the enterococcus cassette chromosome (ECC) element was located in the 3′ region of rlmH and encoded large serine recombinases ccrAB similar to SCCmec. Horizontal transfer of an ECC element termed ECC::cat containing a knock-in cat chloramphenicol resistance determinant occurred in the presence of a conjugative reppLG1 plasmid. We determined the ECC::cat insertion site in the 3′ region of rlmH in the E. faecium recipient by long-read sequencing. ECC::cat also mobilized by homologous recombination through sequence identity between flanking insertion sequence (IS) elements in ECC::cat and the conjugative plasmid. The ccrABEnt genes were found in 69 of 516 E. faecium genomes in GenBank. Full-length ECC elements were retrieved from 32 of these genomes. ECCs were flanked by attR and attL sites of approximately 50 bp. The attECC sequences were found by PCR and sequencing of circularized ECCs in three strains. The genes in ECCs contained an amalgam of common and rare E. faecium genes. Taken together, our data imply that ECC elements act as hot spots for genetic exchange and contribute to the large variation of accessory genes found in E. faecium. IMPORTANCE Enterococcus faecium is a bacterium found in a great variety of environments, ranging from the clinic as a nosocomial pathogen to natural habitats such as mammalian intestines, water, and soil. They are known to exchange genetic material through horizontal gene transfer and recombination, leading to great variability of accessory genes and aiding environmental adaptation. Identifying mobile genetic elements causing sequence variation is important to understand how genetic content variation occurs. Here, a novel genetic island, the enterococcus cassette chromosome, is shown to contain a wealth of genes, which may aid E. faecium in adapting to new environments. The transmission mechanism involves the only two conserved genes within ECC, ccrABEnt, large serine recombinases that insert ECC into the host genome similarly to SCC elements found in staphylococci.

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A mobile genetic element increases bacterial host fitness by manipulating development

10.1101/2020.10.09.328104 ◽

2020 ◽

Author(s):

Joshua M. Jones ◽

Ilana Grinberg ◽

Avigdor Eldar ◽

Alan D. Grossman

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Mobile Genetic Elements ◽

Selective Advantage ◽

Host Cells ◽

Bacterial Host ◽

Host Fitness ◽

Genetic Elements ◽

Necessary And Sufficient ◽

Integrative And Conjugative Element

AbstractHorizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial cargo genes. Uncovering strategies used by mobile genetic elements to benefit host cells is crucial for understanding their stability and spread in populations. We describe a benefit that ICEBs1, an integrative and conjugative element ofBacillus subtilis, provides to its host cells. Activation of ICEBs1conferred a frequency-dependent selective advantage to host cells during two different developmental processes: biofilm formation and sporulation. These benefits were due to inhibition of biofilm-associated gene expression and delayed sporulation by ICEBs1-containing cells, enabling them to exploit their neighbors and grow more prior to development. A single ICEBs1gene,devI(formerlyydcO), was both necessary and sufficient for inhibition of development. Manipulation of host developmental programs allows ICEBs1to increase host fitness, thereby increasing propagation of the element.

Download Full-text