Dynamics of <i>Escherichia coli</i> type I‐E CRISPR spacers over 42 000 years

Savitskaya, Ekaterina; Lopatina, Anna; Medvedeva, Sofia; Kapustin, Mikhail; Shmakov, Sergey; Tikhonov, Alexei; Artamonova, Irena I.; Logacheva, Maria D.; Severinov, Konstantin

doi:10.1111/mec.13961

Cited by 29 publications

(28 citation statements)

References 35 publications

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“…These gene family expansions are often located in the recombinogenic parts of the genome, which could also apply to the phage genomes in our dataset, as the additional ORFs are found upstream of ORF66, which contains a putative ICE (Integrative and The presence of CRISPR/Cas systems has been found in approximately 40% of studied bacterial species 32 , and the molecular mechanisms of different CRISPR systems are under rigorous research 40 . Some repeat-spacer arrays remain relatively constant over millennia 41 , while in some cases no two identical CRISPR loci are found in cells living in close proximity 22 . A study on a closely related species, the fish pathogen Flavobacterium psychrophilum, identified only inactive CRISPR loci across multiple strains 42 .…”

Section: Discussionmentioning

confidence: 99%

Long-term genomic coevolution of host-parasite interaction in the natural environment

Laanto

Hoikkala

Ravantti

et al. 2017

Preprint

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The antagonistic coevolution of parasite infectivity and host resistance alters the biological functionality of species, with effects spanning to communities and ecosystems. Still, studies describing long-term host-parasite coevolutionary dynamics in nature are largely missing.Furthermore, the role of host resistance mechanisms for parasite evolution is poorly understood, necessitating for the molecular and phenotypic characterization of both coevolving parasites and their hosts. We combined long-term field sampling (2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014), in vitro cross-infections and timeshift experiments with bacteriophage whole genome sequencing and bacterial (Flavobacterium columnare) CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) profiling to show the molecular details of the phage-bacterium arms race in the environment. Bacteria were generally resistant to phages from the past and susceptible to phages in the future. The bacterial resistance selected for increased phage infectivity and host range, correlating directly with the expansion of phage genome size by 2656 bp. In the bacterial host, two CRISPR loci were identified: a type II-C locus and an RNA-targeting type VI-B locus. While maintaining a core set of conserved spacers, phage-matching spacers appeared in the variable end of both CRISPR loci over time. The appearance of these CRISPR spacers in the bacterial host often corresponded with arms race -manner molecular changes in the protospacers of the coevolving phage population. However, the phenotypic data indicated that the relative role of constitutive defence may be more important in high phage pressure, highlighting the importance of our findings for understanding microbial community ecology and in the development of phage therapy applications.

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Section: Discussionmentioning

confidence: 99%

Long-term genomic coevolution of host-parasite interaction in the natural environment

Laanto

Hoikkala

Ravantti

et al. 2017

Preprint

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“…In contrast, a comparative analysis of E. coli CRISPR spacers recovered from intestines of a 42 000‐year‐old mammoth with present‐day E. coli did not support intensive change through adaptive acquisition over time (Savitskaya et al . ).…”

Section: Insights On Microbial Adaptation From Patterns Of Local Adapmentioning

confidence: 97%

Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution

2017

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“…2). Furthermore, in Escherichia coli, the only microbe for which the virome can be considered comprehensively characterized, there are virtually no spacers with matches to the known viral genomes, suggesting that the apparently inactive CRISPR arrays in this bacterium have accumulated mismatches to the cognate protospacers that render them unrecognizable (75). Further characterization of the pan-mobilomes of diverse bacteria and measurement of spacer amelioration rates should improve our understanding of the evolution of the CRISPR spacer space and the virus-host arms race.…”

Section: Discussionmentioning

confidence: 99%

The CRISPR Spacer Space Is Dominated by Sequences from Species-Specific Mobilomes

Shmakov

Sitnik

Makarova

et al. 2017

mBio

198

195

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Clustered regularly interspaced short palindromic repeats and CRISPRassociated protein (CRISPR-Cas) systems store the memory of past encounters with foreign DNA in unique spacers that are inserted between direct repeats in CRISPR arrays. For only a small fraction of the spacers, homologous sequences, called protospacers, are detectable in viral, plasmid, and microbial genomes. The rest of the spacers remain the CRISPR "dark matter." We performed a comprehensive analysis of the spacers from all CRISPR-cas loci identified in bacterial and archaeal genomes, and we found that, depending on the CRISPR-Cas subtype and the prokaryotic phylum, protospacers were detectable for 1% to about 19% of the spacers (~7% global average). Among the detected protospacers, the majority, typically 80 to 90%, originated from viral genomes, including proviruses, and among the rest, the most common source was genes that are integrated into microbial chromosomes but are involved in plasmid conjugation or replication. Thus, almost all spacers with identifiable protospacers target mobile genetic elements (MGE). The GC content, as well as dinucleotide and tetranucleotide compositions, of microbial genomes, their spacer complements, and the cognate viral genomes showed a nearly perfect correlation and were almost identical. Given the near absence of self-targeting spacers, these findings are most compatible with the possibility that the spacers, including the dark matter, are derived almost completely from the species-specific microbial mobilomes. IMPORTANCEThe principal function of CRISPR-Cas systems is thought to be protection of bacteria and archaea against viruses and other parasitic genetic elements. The CRISPR defense function is mediated by sequences from parasitic elements, known as spacers, that are inserted into CRISPR arrays and then transcribed and employed as guides to identify and inactivate the cognate parasitic genomes. However, only a small fraction of the CRISPR spacers match any sequences in the current databases, and of these, only a minority correspond to known parasitic elements. We show that nearly all spacers with matches originate from viral or plasmid genomes that are either free or have been integrated into the host genome. We further demonstrate that spacers with no matches have the same properties as those of identifiable origins, strongly suggesting that all spacers originate from mobile elements.KEYWORDS CRISPR-Cas, bacteriophages, mobilome, oligonucleotide composition, spacer acquisition C RISPR-Cas (clustered regularly interspaced palindromic repeats and CRISPRassociated proteins) systems are adaptive (acquired) immune systems of archaea and bacteria that store memory of past encounters with foreign DNA in unique spacer Citation Shmakov SA, Sitnik V, Makarova KS, Wolf YI, Severinov KV, Koonin EV. 2017. The CRISPR spacer space is dominated by sequences from species-specific mobilomes.

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Dynamics of Escherichia coli type I‐E CRISPR spacers over 42 000 years

Cited by 29 publications

References 35 publications

Long-term genomic coevolution of host-parasite interaction in the natural environment

Long-term genomic coevolution of host-parasite interaction in the natural environment

Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution

The CRISPR Spacer Space Is Dominated by Sequences from Species-Specific Mobilomes

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