Analysis of the CRISPR-Cas system in bacteriophages active on epidemic strains of Vibrio cholerae in Bangladesh

Naser, Iftekhar Bin; Hoque, M. Mozammel; Nahid, M. Ausrafuggaman; Tareq, Tokee M.; Rocky, M. Kamruzzaman; Faruque, Shah M.

doi:10.1038/s41598-017-14839-2

Cited by 34 publications

(46 citation statements)

References 42 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…To evaluate if the fixation of CRISPR in ICP1 is necessitated by co-circulating PLE in epidemic V. cholerae , we determined the prevalence of PLE over the same near two-decade long period in Dhaka. Combined with previous analyses (12,21), we observed an increase in the prevalence of PLE(+) V. cholerae in epidemic sampling over time (Fig. 1c).…”

Section: Resultssupporting

confidence: 86%

“…We set out to compare ICP1 and PLE from contemporary cholera patient stool samples to previously identified isolates from the International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B) in Dhaka, Bangladesh (13,21). We isolated eight new ICP1 isolates from cholera patient stool samples collected between 2015-2017 and found that all isolates harbor CRISPR-Cas.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Competition between mobile genetic elements drives optimization of a phage-encoded CRISPR-Cas system: Insights from a natural arms-race

McKitterick¹,

LeGault²,

Angermeyer³

et al. 2018

Preprint

View full text Add to dashboard Cite

17CRISPR-Cas systems function as adaptive immune systems by acquiring nucleotide sequences 18 called spacers that mediate sequence-specific defense against competitors. Uniquely, the 19 phage ICP1 encodes a Type I-F CRISPR-Cas system that is deployed to target and overcome 20 PLE, a mobile genetic element with anti-phage activity in Vibrio cholerae. Here, we exploit the 21 arms race between ICP1 and PLE to examine spacer acquisition and interference under 22 laboratory conditions to reconcile findings from wild populations. Natural ICP1 isolates encode 23 multiple spacers directed against PLE, but we find that single spacers do not equally interfere 24 with PLE mobilization. High-throughput sequencing to assay spacer acquisition reveals that 25 ICP1 can also acquire spacers that target the V. cholerae chromosome. We find that targeting 26 the V. cholerae chromosome proximal to PLE is sufficient to block PLE and propose a model in 27 which indirect chromosomal spacers are able to circumvent PLE by Cas2-3-mediated 28 processive degradation of the V. cholerae chromosome before PLE mobilization. Generally, 29 laboratory acquired spacers are much more diverse than the subset of spacers maintained by 30

show abstract

Section: Resultssupporting

confidence: 86%

Section: Resultsmentioning

confidence: 99%

Competition between mobile genetic elements drives optimization of a phage-encoded CRISPR-Cas system: Insights from a natural arms-race

McKitterick¹,

LeGault²,

Angermeyer³

et al. 2018

Preprint

View full text Add to dashboard Cite

show abstract

“…These ranged from occurrences in 18 genomes (n=12) to singletons (n=14) (Figure 3) with several patterns of accessory ORF co-occurrence (Table S2). The most obvious example was the CRISPR-Cas locus which was previously known to reside in 8 of these genomes [13,15] and confirmed through our annotation methods. Other examples of sequential ORF co-occurrence included a locus containing ORFs 115, 116, 117, 117.1 and 118 which were found in the same five genomes, ORFs 160, 162, 163 in a different set of five overlapping genomes and ORFs 222, 223, 225 in 15 genomes.…”

Section: Resultssupporting

confidence: 69%

“…Previous work has identified a V. cholera O1-specific [10] lytic myoviridae bacteriophage (ICP1) to be of particular interest in this system [11]. In Bangladesh, ICP1 has been found in water samples [12,13] and it has been identified as the dominant phage in cholera patient stool samples since 2001 [11]. The persistence of this phage over time indicates that V. cholerae has strategies to limit ICP1 predation, and that ICP1 can evolve to overcome such defenses.…”

Section: Introductionmentioning

confidence: 99%

Analysis of 19 Highly Conserved Vibrio cholerae Bacteriophages Isolated from Environmental and Patient Sources Over a Twelve-Year Period

Angermeyer

Das

Singh

et al. 2018

Preprint

View full text Add to dashboard Cite

The Vibrio cholerae biotype 'El Tor' is responsible for all current epidemic and endemic 12 cholera outbreaks worldwide. These outbreaks are clonal and are hypothesized to originate from 13 the coastal areas near the Bay of Bengal where the lytic bacteriophage ICP1 specifically preys upon 14 these pathogenic outbreak strains. ICP1 has also been the dominant bacteriophage found in 15 cholera patient stool since 2001. However, little is known about its genomic differences between 16 ICP1 strains collected over time. Here we elucidate the pan-genome and phylogeny of ICP1 strains 17 by aligning, annotating and analyzing the genomes of 19 distinct isolates collected between 2001 18 and 2012. Our results reveal that ICP1 isolates are highly conserved and possess a large 19 core-genome as well as a smaller, somewhat flexible accessory-genome. Despite its overall 20 conservation, ICP1 strains have managed to acquire a number of unknown genes as well as a 21 CRISPR-Cas system, which is known to be critical for its ongoing struggle for co-evolutionary 22 dominance over its host. This study describes a foundation on which to construct future molecular 23 and bioinformatic studies of this V. cholerae-associated bacteriophages. 24 25 phage 26 27 42 environment where they can outnumber their prokaryotic hosts by several orders of magnitude [8]. 43As such, bacteriophage play a key role in the evolution of their hosts through both selection and 44 phage-mediated lateral gene transfer [9]. These processes are likely to be very important to V. 45 cholerae strain evolution in the Bay of Bengal as well. Previous work has identified a V. cholerae 46 2 of 11 O1-specific [10] lytic myoviridae bacteriophage (ICP1) to be of particular interest in this system [11]. 47In Bangladesh, ICP1 has been found in water samples [12,13] and it has been identified as the 48 dominant phage in cholera patient stool samples since 2001 [11]. The persistence of this phage over 49 time indicates that V. cholerae has strategies to limit ICP1 predation, and that ICP1 can evolve to 50 overcome such defenses. Indeed, from this natural genetic laboratory, several complex and 51 surprising adaptations/acquisitions have occurred in the race for survival between V. cholerae and 52 ICP1. These include self-mobilizing chromosomal islands that can provide a rapid and efficient 53 response to ICP1 infection [14] and the first known example of a bacteriophage-encoded 54 CRISPR-Cas system [15]. Initial characterization of eight ICP1 isolates collected between 2001-2011 55 noted the relative low level of diversity and lack of major genomic rearrangements, deletions or 56 insertions [11] (with the exception of its remarkable CRISPR-Cas acquisition [15]). Here we build 57 upon the initial characterization of ICP1 to perform a comparative genomic analysis on 19 58 individual ICP1 isolates to reconstruct their phylogenetic relationships over time, identify the core 59 and accessory genomes, and infer possible gene function where possible. 60V. cholerae is an organism that a...

show abstract

“…Because of ICP3’s fickle nature in water, it is possible that maintenance of ICP3 in Bangladesh relies primarily upon rapid transmission between people such as occurs within households (32). Of 29 sequences reported for environmental V. cholerae phages (11, 25, 29, 33), 41% corresponded to ICP3-like phages. This result is striking, since our model does not support the notion that ICP3 can replicate in nutrient-limiting aquatic environments.…”

Section: Discussionmentioning

confidence: 99%

Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment

Camilli

Silva-Valenzuela

2018

Preprint

View full text Add to dashboard Cite

20Vibrio cholerae, the causative agent of cholera, has reservoirs in fresh and brackish 21 water where it interacts with virulent bacteriophages. Phages are the most abundant 22 certain niches or stages of the host bacterial life cycle. Unveiling the phage/bacterial 44 interactions in their natural setting is important to the understanding of cholera outbreaks 45 and could be ultimately used to help develop a method for outbreak prediction and/or 46 control. 47 48 \body 49

show abstract

Analysis of the CRISPR-Cas system in bacteriophages active on epidemic strains of Vibrio cholerae in Bangladesh

Cited by 34 publications

References 42 publications

Competition between mobile genetic elements drives optimization of a phage-encoded CRISPR-Cas system: Insights from a natural arms-race

Competition between mobile genetic elements drives optimization of a phage-encoded CRISPR-Cas system: Insights from a natural arms-race

Analysis of 19 Highly Conserved Vibrio cholerae Bacteriophages Isolated from Environmental and Patient Sources Over a Twelve-Year Period

Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment

Contact Info

Product

Resources

About