The arms race between bacteria and their phage foes

Hampton, Hannah G; Watson, Bridget N. J.; Fineran, Peter C.

doi:10.1038/s41586-019-1894-8

Cited by 659 publications

(542 citation statements)

References 176 publications

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“…Prokaryotes have evolved several strategies to provide defense against mobile genetic elements, such as viruses and plasmids ( 1 ). One mechanism is CRISPR-Cas immunity ( 2 ), which consists of CRISPR array(s), which store foreign sequences as spacers ( 3 ), and cas genes that encode proteins required for adaptive immunity ( 4, 5 ).…”

Section: Main Textmentioning

confidence: 99%

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Diverse CRISPR-Cas complexes require independent translation of small and large subunits from a single gene

McBride

Schwartz

Kumar

et al. 2020

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CRISPR-Cas adaptive immune systems provide bacteria and archaea with defense16 against their viruses and other mobile genetic elements 1 . CRISPR-Cas immunity 17 involves the formation of ribonucleoprotein complexes that specifically bind and 18 degrade foreign nucleic acids 2,3 . Despite advances in the biotechnological exploitation 19 of select systems, multiple CRISPR-Cas types remain uncharacterized 4 . Here, we 20 investigated a type I-D system from Synechocystis and revealed the Cascade complex, 21 which is required for interference, forms a hybrid ribonucleoprotein complex that is 22 structurally and genetically related to both type I and III systems 5-8 . Surprisingly, the 23 type I-D complex contained multiple functionally-important small subunit proteins 24 encoded from an internal in-frame translation initiation site within the large subunit 25 gene, cas10d. Structural analysis revealed that these small subunits bound the 26 complex similarly to Cas11 small subunits in other type I and III systems, where they 27 are encoded as a separate gene. We show that internal translation of small subunits 28 from within large subunit genes is conserved across diverse type I-D, I-B and I-C 29 systems, which account for ~23% of all sequenced CRISPR-Cas systems 4 . Indeed, we 30 demonstrate that small subunits are expressed from within the cas8c large subunit 31 gene in the Desulfovibrio vulgaris type I-C system. Our work reveals an unexpected 32 aspect of CRISPR-Cas evolution and expansion of the coding potential from within 1 single cas genes. 2 3

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Section: Main Textmentioning

confidence: 99%

“… CRISPR-Cas adaptive immune systems provide bacteria and archaea with defense against their viruses and other mobile genetic elements 1 . CRISPR-Cas immunity involves the formation of ribonucleoprotein complexes that specifically bind and degrade foreign nucleic acids 2,3 .…”

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confidence: 99%

Diverse CRISPR-Cas complexes require independent translation of small and large subunits from a single gene

McBride

Schwartz

Kumar

et al. 2020

Preprint

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“…CRISPR-Cas systems are one among several mechanisms that have evolved in bacteria to fight phages [73, 77]. In its natural habitat, Gordonia would be protected by several lines of defense, including the protecting effect of EPS and spatial heterogeneity of the matrix.…”

Section: Discussionmentioning

confidence: 99%

Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system

Guerrero

Pérez

Orellana

et al. 2020

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Bacterial viruses are widespread and abundant across natural and engineered habitats. They influence ecosystem functioning through interactions with their hosts. Laboratory studies of phage-host pairs have advanced our understanding of phenotypic and genetic diversification in bacteria and phages. However, the dynamics of phage-host interactions has been seldom recorded in complex natural environments. We conducted an observational metagenomic study of the dynamics of interaction between Gordonia and their phages using a three-year data series of samples collected from a full-scale wastewater treatment plant. The aim was to obtain a comprehensive picture of the coevolution dynamics in naturally evolving populations at relatively high time resolution. Co-evolution was followed by monitoring changes over time in the CRISPR loci of Gordonia metagenome-assembled genome, and reciprocal changes in the viral genome. Genome-wide analysis indicated low strain variability of Gordonia, and almost clonal conservation of the trailer-end of the CRISPR loci. Incorporation of newer spacers gave rise to multiple coexisting bacterial populations. A host population containing a CRISPR array variant, which did not contain spacers against the coexisting phages, accounted for more than half of the total host abundance in the majority of samples. Phages genome co-evolved by introducing directional changes, with no preference for mutations within the protospacer and PAM regions. Metagenomic reconstruction of time-resolved variants of host and virus genomes revealed how selection operates at the population level. In activated sludge, it differed from the arms-race observed in nutrient rich media and resembled the fluctuating selection dynamics observed in natural environments.

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“…Like all other prokaryotic defense systems, CRISPR-Cas loci evolve rapidly in a constant arms race with their mobile genetic element foes (Hampton, Watson, and Fineran 2020) . The resultant evolutionary tension has led to a remarkable diversification of CRISPR-Cas systems, which, together with the apparently frequent exchange of components and lack of a universal marker gene across systems , greatly challenges the development of a unified classification scheme.…”

Section: Introductionmentioning

confidence: 99%

CRISPRCasTyper: An automated tool for the identification, annotation and classification of CRISPR-Cas loci

Russel

Pinilla‐Redondo

Mayo-Muñoz

et al. 2020

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CRISPR-Cas loci encode for highly diversified prokaryotic adaptive defense systems that have recently become popular for their applications in gene editing and beyond. The increasing demand for bioinformatic tools that systematically detect and classify CRISPR-Cas systems has been largely challenged by their complex dynamic nature and rapidly expanding classification. Here, we developed CRISPRCasTyper, a new automated software tool with improved capabilities for identifying and typing CRISPR arrays and cas loci across prokaryotic sequences, based on the latest classification and nomenclature (39 subtypes/variants) (Makarova et al. 2020;Pinilla-Redondo et al. 2019) . As a novel feature, CRISPRCasTyper uses a machine learning approach to subtype CRISPR arrays based on the sequences of the direct repeats. This allows the typing of orphan and distant arrays which, for example, are commonly observed in fragmented metagenomic assemblies. Furthermore, the tool provides a graphical output, where CRISPRs and cas operon arrangements are visualized in the form of colored gene maps, thus aiding annotation of partial and novel systems through synteny. Moreover, CRISPRCasTyper can resolve hybrid CRISPR-Cas systems and detect loci spanning the ends of sequences with a circular topology, such as complete genomes and plasmids. CRISPRCasTyper was benchmarked against a manually curated set of 31 subtypes/variants with a median accuracy of 98.6%. Altogether, we present an up-to-date and freely available software pipeline for significantly improved automated predictions of CRISPR-Cas loci across genomic sequences. ImplementationCRISPRCasTyper is available through conda and PyPi under the MIT license ( https://github.com/Russel88/CRISPRCasTyper ), and is also available as a web server

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The arms race between bacteria and their phage foes

Cited by 659 publications

References 176 publications

Diverse CRISPR-Cas complexes require independent translation of small and large subunits from a single gene

Diverse CRISPR-Cas complexes require independent translation of small and large subunits from a single gene

Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system

CRISPRCasTyper: An automated tool for the identification, annotation and classification of CRISPR-Cas loci

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