The phage‐host arms race: Shaping the evolution of microbes

Stern, Adi; Sorek, Rotem

doi:10.1002/bies.201000071

Cited by 446 publications

(358 citation statements)

References 115 publications

(115 reference statements)

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“…2) could be a potential candidate. Another role for this modification could be to provide resistance to restriction systems, essentially acting as an antirestriction system (47). The phage 9g DNA is resistant to most restriction enzymes tested (38), suggesting the presence of modified bases inhibits recognition or cleavage by these enzymes.…”

Section: 46)mentioning

confidence: 99%

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Thiaville

Kellner

Yuan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

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The discovery of ∼20-kb gene clusters containing a family of paralogs of tRNA guanosine transglycosylase genes, called tgtA5, alongside 7-cyano-7-deazaguanine (preQ 0 ) synthesis and DNA metabolism genes, led to the hypothesis that 7-deazaguanine derivatives are inserted in DNA. This was established by detecting 2'-deoxy-preQ 0 and 2'-deoxy-7-amido-7-deazaguanosine in enzymatic hydrolysates of DNA extracted from the pathogenic, Gram-negative bacteria Salmonella enterica serovar Montevideo. These modifications were absent in the closely related S. enterica serovar Typhimurium LT2 and from a mutant of S. Montevideo, each lacking the gene cluster. This led us to rename the genes of the S. Montevideo cluster as dpdA-K for 7-deazapurine in DNA. Similar gene clusters were analyzed in ∼150 phylogenetically diverse bacteria, and the modifications were detected in DNA from other organisms containing these clusters, including Kineococcus radiotolerans, Comamonas testosteroni, and Sphingopyxis alaskensis. Comparative genomic analysis shows that, in Enterobacteriaceae, the cluster is a genomic island integrated at the leuX locus, and the phylogenetic analysis of the TgtA5 family is consistent with widespread horizontal gene transfer. Comparison of transformation efficiencies of modified or unmodified plasmids into isogenic S. Montevideo strains containing or lacking the cluster strongly suggests a restriction-modification role for the cluster in Enterobacteriaceae. Another preQ 0 derivative, 2'-deoxy-7-formamidino-7-deazaguanosine, was found in the Escherichia coli bacteriophage 9g, as predicted from the presence of homologs of genes involved in the synthesis of the archaeosine tRNA modification. These results illustrate a deep and unexpected evolutionary connection between DNA and tRNA metabolism.DNA modification | restriction-modification | 7-deazaguanine | comparative genomics | queuosine H ypermodifications of DNA requiring more than one synthetic enzyme are not as prevalent and chemically diverse as RNA hypermodifications, but around a dozen have been identified in DNA to date (1). The functions of most DNA hypermodifications are still not known, but some have roles in protection against restriction enzymes, whereas others affect thermal stability temperature, DNA packaging, or transcription regulation (2). For example, the hypermodified DNA base β-D-glucosyl-hydroxymethyluracil, or base J, is an epigenetic factor that regulates Pol II transcription initiation in kinetoplastids of trypanosomes (3). The recently discovered phosphorothioate (PT) modification of the DNA backbone in bacteria was found to perform different functions in different organisms (4-6). In Salmonella Cerro 87, PT occurs on each strand of a GAAC/GTTC motif as part of a restriction-modification (R-M) system, whereas in Vibrio cyclitrophicus FF75, which lacks PT restriction enzymes, PT occurs on one strand of C ps CA motifs, and the function remains unclear (6). In 2013, Iyer et al. described the computational prediction of 12 novel DNA hypermodificat...

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Section: 46)mentioning

confidence: 99%

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Thiaville

Kellner

Yuan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

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“…These guides a dedicated set of CRISPR-associated (Cas) proteins to their targets during cellular surveillance (Marraffini and Sontheimer 2010;van der Oost et al 2009). Indeed, upon reinfection, when the DNA or in some cases mRNA of remembered invaders is identified, the CRISPR-Cas system binds to invading phage DNA resulting in the degradation of the phage genome sequence (Stern and Sorek 2011). (Color figure online) By contrast, in the second approach, named ''indirect mDNA extraction'', the environmental samples need to be physically and mechanically treated before cell lysis.…”

Section: Crisprmentioning

confidence: 99%

Metagenomics of microbial and viral life in terrestrial geothermal environments

Strazzulli

Fusco

Cobucci‐Ponzano

et al. 2017

Rev Environ Sci Biotechnol

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Geothermally heated regions of Earth, such as terrestrial volcanic areas (fumaroles, hot springs, and geysers) and deep-sea hydrothermal vents, represent a variety of different environments populated by extremophilic archaeal and bacterial microorganisms. Since most of these microbes thriving in such harsh biotopes, they are often recalcitrant to cultivation; therefore, ecological, physiological and phylogenetic studies of these microbial populations have been hampered for a long time. More recently, culture-independent methodologies coupled with the fast development of next generation sequencing technologies as well as with the continuous advances in computational biology, have allowed the production of large amounts of metagenomic data. Specifically, these approaches have assessed the phylogenetic composition and functional potential of microbial consortia thriving within these habitats, shedding light on how extreme physico-chemical conditions and biological interactions have shaped such microbial communities. Metagenomics allowed to better understand that the exposure to an extreme range of selective pressures in such severe environments, accounts for genomic flexibility and metabolic versatility of microbial and viral communities, and makes extreme-and hyper-thermophiles suitable for bioprospecting purposes, representing an interesting source for novel thermostable proteins that can be potentially used in several industrial processes.Keywords Hyperthermophiles Á Geothermal environments Á Microbial and viral metagenomics Á CRISPR Á Enzyme discovery BackgroundHot springs populated by extreme thermophiles (T opt : 65-79°C) and hyperthermophiles (T opt [ 80°C) (DeCastro et al. 2016) are very diverse and some of them show combinations of extreme chemo-physical conditions, such as temperature, acidic or alkaline pHs, high pressure, and high concentrations of salts and heavy metals (López-López et al. 2013). As with all studies of environmental microbiology, our understanding of the composition, functional and physiological dynamics, and evolution of extreme-and hyper-thermophilic microbial consortia has lagged A. Strazzulli Á M. Moracci Á P. Contursi

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“…From the perspective of the bacteria, survival entails the selection of cells that are resistant to infection, preventing viral production and enabling the continuation of the cell lineage. Resistance mechanisms include passively acquired spontaneous mutations in cell surface molecules that prevent phage entry into the cell and other mechanisms that actively terminate phage infection intracellularly, such as restriction-modification systems and acquired resistance by CRISPR-Cas systems (21,22). Mutations in the phage can also occur that circumvent these host defenses and enable the phage to infect the recently emerged resistant bacterium (23).…”

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confidence: 99%

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Avrani

Lindell

2015

Proc. Natl. Acad. Sci. U.S.A.

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Prochlorococcus is an abundant marine cyanobacterium that grows rapidly in the environment and contributes significantly to global primary production. This cyanobacterium coexists with many cyanophages in the oceans, likely aided by resistance to numerous co-occurring phages. Spontaneous resistance occurs frequently in Prochlorococcus and is often accompanied by a pleiotropic fitness cost manifested as either a reduced growth rate or enhanced infection by other phages. Here, we assessed the fate of a number of phage-resistant Prochlorococcus strains, focusing on those with a high fitness cost. We found that phage-resistant strains continued evolving toward an improved growth rate and a narrower resistance range, resulting in lineages with phenotypes intermediate between those of ancestral susceptible wild-type and initial resistant substrains. Changes in growth rate and resistance range often occurred in independent events, leading to a decoupling of the selection pressures acting on these phenotypes. These changes were largely the result of additional, compensatory mutations in noncore genes located in genomic islands, although genetic reversions were also observed. Additionally, a mutator strain was identified. The similarity of the evolutionary pathway followed by multiple independent resistant cultures and clones suggests they undergo a predictable evolutionary pathway. This process serves to increase both genetic diversity and infection permutations in Prochlorococcus populations, further augmenting the complexity of the interaction network between Prochlorococcus and its phages in nature. Last, our findings provide an explanation for the apparent paradox of a multitude of resistant Prochlorococcus cells in nature that are growing close to their maximal intrinsic growth rates.cyanobacteria | cyanophage | resistance | Prochlorococcus | virus

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The phage‐host arms race: Shaping the evolution of microbes

Cited by 446 publications

References 115 publications

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Metagenomics of microbial and viral life in terrestrial geothermal environments

Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

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