scholarly journals Transductomics: sequencing-based detection and analysis of transduced DNA in pure cultures and microbial communities

Microbiome ◽  
2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Manuel Kleiner ◽  
Brian Bushnell ◽  
Kenneth E. Sanderson ◽  
Lora V. Hooper ◽  
Breck A. Duerkop
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Communities ◽  
Microbial Evolution ◽  
Model Systems ◽  
Intestinal Microbiome ◽  
Mobile Dna ◽  
Pure Cultures ◽  
Taxonomic Range ◽  
Taxonomic Groups

Abstract Background Horizontal gene transfer (HGT) plays a central role in microbial evolution. Our understanding of the mechanisms, frequency, and taxonomic range of HGT in polymicrobial environments is limited, as we currently rely on historical HGT events inferred from genome sequencing and studies involving cultured microorganisms. We lack approaches to observe ongoing HGT in microbial communities. Results To address this knowledge gap, we developed a DNA sequencing-based “transductomics” approach that detects and characterizes microbial DNA transferred via transduction. We validated our approach using model systems representing a range of transduction modes and show that we can detect numerous classes of transducing DNA. Additionally, we show that we can use this methodology to obtain insights into DNA transduction among all major taxonomic groups of the intestinal microbiome. Conclusions The transductomics approach that we present here allows for the detection and characterization of genes that are potentially transferred between microbes in complex microbial communities at the time of measurement and thus provides insights into real-time ongoing horizontal gene transfer. This work extends the genomic toolkit for the broader study of mobile DNA within microbial communities and could be used to understand how phenotypes spread within microbiomes.

scholarly journals Microbial DNA on the move: sequencing based detection and analysis of transduced DNA in pure cultures and microbial communities

2020 ◽  
Author(s):  
Manuel Kleiner ◽  
Brian Bushnell ◽  
Kenneth E. Sanderson ◽  
Lora V. Hooper ◽  
Breck A. Duerkop
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Communities ◽  
Microbial Evolution ◽  
Model Systems ◽  
Intestinal Microbiome ◽  
Mobile Dna ◽  
Pure Cultures ◽  
Taxonomic Groups ◽  
Microbial Dna

AbstractHorizontal gene transfer (HGT) plays a central role in microbial evolution. Our understanding of the mechanisms, frequency and taxonomic range of HGT in polymicrobial environments is limited, as we currently rely on historical HGT events inferred from genome sequencing and studies involving cultured microorganisms. We lack approaches to observe ongoing HGT in microbial communities. To address this knowledge gap, we developed a DNA sequencing based “transductomics” approach that detects and characterizes microbial DNA transferred via transduction. We validated our approach using model systems representing a range of transduction modes and show that we can detect numerous classes of transducing DNA. Additionally, we show that we can use this methodology to obtain insights into DNA transduction among all major taxonomic groups of the intestinal microbiome. This work extends the genomic toolkit for the broader study of mobile DNA within microbial communities and could be used to understand how phenotypes spread within microbiomes.Significance StatementMicrobes can rapidly evolve new capabilities by acquiring genes from other organisms through a process called horizontal gene transfer (HGT). HGT occurs via different routes, one of which is by the transfer of DNA carried by microbe infecting viruses (phages) or virus-like agents. This process is called transduction and has primarily been studied in the lab using pure cultures or indirectly in environmental communities by analyzing signatures in microbial genomes revealing past transduction events. The transductomics approach that we present here, allows for the detection and characterization of genes that are potentially transferred between microbes in complex microbial communities at the time of measurement and thus provides insights into real-time ongoing horizontal gene transfer.

scholarly journals Experimental approaches to tracking mobile genetic elements in microbial communities

2020 ◽  
Vol 44 (5) ◽  
pp. 606-630 ◽  
Author(s):  
Christina C Saak ◽  
Cong B Dinh ◽  
Rachel J Dutton
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Communities ◽  
Mobile Genetic Elements ◽  
Mobile Elements ◽  
Microbial Evolution ◽  
Fermented Food ◽  
Chromosome Conformation ◽  
Genetic Elements ◽  
Experimental Approaches

ABSTRACT Horizontal gene transfer is an important mechanism of microbial evolution and is often driven by the movement of mobile genetic elements between cells. Due to the fact that microbes live within communities, various mechanisms of horizontal gene transfer and types of mobile elements can co-occur. However, the ways in which horizontal gene transfer impacts and is impacted by communities containing diverse mobile elements has been challenging to address. Thus, the field would benefit from incorporating community-level information and novel approaches alongside existing methods. Emerging technologies for tracking mobile elements and assigning them to host organisms provide promise for understanding the web of potential DNA transfers in diverse microbial communities more comprehensively. Compared to existing experimental approaches, chromosome conformation capture and methylome analyses have the potential to simultaneously study various types of mobile elements and their associated hosts. We also briefly discuss how fermented food microbiomes, given their experimental tractability and moderate species complexity, make ideal models to which to apply the techniques discussed herein and how they can be used to address outstanding questions in the field of horizontal gene transfer in microbial communities.

Horizontal Gene Transfer in Microbial Evolution

2018 ◽  
pp. 527-533
Author(s):  
Johann Peter Gogarten ◽  
R. Thane Papke
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Evolution

scholarly journals Variability in Assembly of Degradation Operons for Naphthalene and its derivative, Carbaryl, Suggests Mobilization through Horizontal Gene Transfer

Genes ◽  
2019 ◽  
Vol 10 (8) ◽  
pp. 569 ◽  
Author(s):  
Phale ◽  
Shah ◽  
Malhotra
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Food Web ◽  
Microbial Communities ◽  
Metabolic Pathways ◽  
Anthropogenic Activities ◽  
Genetic Material ◽  
Genomic Islands ◽  
Biochemical Pathways ◽  
Integrative Conjugative Elements

In the biosphere, the largest biological laboratory, increased anthropogenic activities have led microbes to evolve and adapt to the changes occurring in the environment. Compounds, specifically xenobiotics, released due to such activities persist in nature and undergo bio-magnification in the food web. Some of these compounds act as potent endocrine disrupters, mutagens or carcinogens, and therefore their removal from the environment is essential. Due to their persistence, microbial communities have evolved to metabolize them partially or completely. Diverse biochemical pathways have evolved or been assembled by exchange of genetic material (horizontal gene transfer) through various mobile genetic elements like conjugative and non-conjugative plasmids, transposons, phages and prophages, genomic islands and integrative conjugative elements. These elements provide an unlimited opportunity for genetic material to be exchanged across various genera, thus accelerating the evolution of a new xenobiotic degrading phenotype. In this article, we illustrate examples of the assembly of metabolic pathways involved in the degradation of naphthalene and its derivative, Carbaryl, which are speculated to have evolved or adapted through the above-mentioned processes.

scholarly journals Horizontal Gene Transfer Can Help Maintain the Equilibrium of Microbial Communities

2017 ◽  
Author(s):  
Yuhang Fan ◽  
Yandong Xiao ◽  
Babak Momeni ◽  
Yang-Yu Liu
Keyword(s):  
Population Dynamics ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Communities ◽  
Transfer Rate ◽  
Species Coexistence ◽  
Focal Points ◽  
Dynamics Model ◽  
Population Dynamics Model ◽  
Evolutionary Advantage

Horizontal gene transfer and species coexistence are two focal points in the study of microbial communities. The evolutionary advantage of horizontal gene transfer has not been well-understood and is constantly being debated. Here we propose a simple population dynamics model based on the frequency-dependent interactions between different genotypes to evaluate the influence of horizontal gene transfer on microbial communities. We find that both structural stability and robustness of the microbial community are strongly affected by the gene transfer rate and direction. An optimal gene flux can stablize the ecosystem, helping it recover from disturbance and maintain the species coexistence.

scholarly journals Diverse Viruses in Deep-Sea Hydrothermal Vent Fluids Have Restricted Dispersal across Ocean Basins

mSystems ◽  
2021 ◽  
Author(s):  
Elaina Thomas ◽  
Rika E. Anderson ◽  
Viola Li ◽  
L. Jenni Rogan ◽  
Julie A. Huber
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Communities ◽  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Viral Ecology ◽  
Unique Nature

Viruses play important roles in manipulating microbial communities and their evolution in the ocean, yet not much is known about viruses in deep-sea hydrothermal vents. However, viral ecology and evolution are of particular interest in hydrothermal vent habitats because of their unique nature: previous studies have indicated that most viruses in hydrothermal vents are temperate rather than lytic, and it has been established that rates of horizontal gene transfer (HGT) are particularly high among thermophilic vent microbes, and viruses are common vectors for HGT.

scholarly journals Novel “Superspreader” Bacteriophages Promote Horizontal Gene Transfer by Transformation

mBio ◽  
2017 ◽  
Vol 8 (1) ◽  
Author(s):  
Eric C. Keen ◽  
Valery V. Bliskovsky ◽  
Francisco Malagon ◽  
James D. Baker ◽  
Jeffrey S. Prince ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Antibiotic Resistance ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Microbial Evolution ◽  
Phage Infection ◽  
Resistant Bacteria ◽  
Natural Environments ◽  
Plasmid Transformation ◽  
Isolation And Characterization

ABSTRACT Bacteriophages infect an estimated 10 23 to 10 25 bacterial cells each second, many of which carry physiologically relevant plasmids (e.g., those encoding antibiotic resistance). However, even though phage-plasmid interactions occur on a massive scale and have potentially significant evolutionary, ecological, and biomedical implications, plasmid fate upon phage infection and lysis has not been investigated to date. Here we show that a subset of the natural lytic phage population, which we dub “superspreaders,” releases substantial amounts of intact, transformable plasmid DNA upon lysis, thereby promoting horizontal gene transfer by transformation. Two novel Escherichia coli phage superspreaders, SUSP1 and SUSP2, liberated four evolutionarily distinct plasmids with equal efficiency, including two close relatives of prominent antibiotic resistance vectors in natural environments. SUSP2 also mediated the extensive lateral transfer of antibiotic resistance in unbiased communities of soil bacteria from Maryland and Wyoming. Furthermore, the addition of SUSP2 to cocultures of kanamycin-resistant E. coli and kanamycin-sensitive Bacillus sp. bacteria resulted in roughly 1,000-fold more kanamycin-resistant Bacillus sp. bacteria than arose in phage-free controls. Unlike many other lytic phages, neither SUSP1 nor SUSP2 encodes homologs to known hydrolytic endonucleases, suggesting a simple potential mechanism underlying the superspreading phenotype. Consistent with this model, the deletion of endonuclease IV and the nucleoid-disrupting protein ndd from coliphage T4, a phage known to extensively degrade chromosomal DNA, significantly increased its ability to promote plasmid transformation. Taken together, our results suggest that phage superspreaders may play key roles in microbial evolution and ecology but should be avoided in phage therapy and other medical applications. IMPORTANCE Bacteriophages (phages), viruses that infect bacteria, are the planet’s most numerous biological entities and kill vast numbers of bacteria in natural environments. Many of these bacteria carry plasmids, extrachromosomal DNA elements that frequently encode antibiotic resistance. However, it is largely unknown whether plasmids are destroyed during phage infection or released intact upon phage lysis, whereupon their encoded resistance could be acquired and manifested by other bacteria (transformation). Because phages are being developed to combat antibiotic-resistant bacteria and because transformation is a principal form of horizontal gene transfer, this question has important implications for biomedicine and microbial evolution alike. Here we report the isolation and characterization of two novel Escherichia coli phages, dubbed “superspreaders,” that promote extensive plasmid transformation and efficiently disperse antibiotic resistance genes. Our work suggests that phage superspreaders are not suitable for use in medicine but may help drive bacterial evolution in natural environments.

Sign in / Sign up

Export Citation Format

Share Document