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Lecture 24: CRISPR-Cas Immunity

Today

  • How do bacteria become immune to phages? CRISPR-Cas9 of course.

  • What are the molecular mechanisms of CRISPR-Cas9 immunity?

  • How is this system used for genome engineering?

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Remember the Luria-Delbrück Experiment

Inoculate cells onto plate with phage

Small number of colonies will grow

Inoculate these cells onto phage plate

Many more colonies!

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Remember the Luria-Delbrück Experiment

When we add the bacterial cells to the phage plate, does that

  1. Induce the mutation?��Or�
  2. Are the mutations pre-existing and the phage plate simply selects for them?

T1 phage

E. coli

How was did they answer the question?

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The two scenarios will have different variances in the number of resistant colonies!

Small variance

Large variance

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The two scenarios will have different variances in the number of resistant colonies!

Experimental data

Expected number assuming pre-existing, spontaneous mutations

Long tail!

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The two scenarios will have different variances in the number of resistant colonies!

Likely scenario

Small variance

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But why not have a way to acquire immunity?

We can do it

Can bacteria?

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

Cas1-Cas2

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

Cas1-Cas2

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

Cas1-Cas2

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How can bacteria acquire immunity to phages?

Phage DNA

Bacterial DNA

Cas1-Cas2

The bacterium now has part of the phage DNA in its own genome???

Let’s take a closer look at this locus.

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The CRISPR locus

Phage DNA. Called “spacers”.

Spaced out repeat sequences.

Clustered regularly interspersed short palindromic repeats

cas genes (CRISPR associated genes, mostly nucleic acid processing genes like nucleases, etc)

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What happens when an encoded phage attempts to infect?

cas genes

Phage sequences

infecting phage genome

Cas proteins

phage-complementary RNAS and “guide” RNAs

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What happens when an encoded phage attempts to infect?

cas genes

Phage sequences

infecting phage genome

Cas proteins

  1. Cas proteins form a complex that can recognize the RNA hairpin
  2. RNA-protein complex recognizes foreign phage DNA
  3. Cas proteins (e.g. Cas9) cuts phage DNA, preventing replication

phage-complementary RNAS and “guide” RNAs

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Cells use multiple types of Cas systems

(+others)

Most famous because it is used for gene editing

Most common

CRISPR systems all search for a short nucleotide sequence called the protospacer-adjacent motif, or PAM, which is short enough to be found in any genome (2-5 bases)

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CRISPR systems impart acquired, heritable immunity!

Bacterial genome

CRISPR spacer

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CRISPR-Immune cells can grow in the presence of phage

CRISPR immunity

Non-functioning CRISPR

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How did researchers discover CRISPR immunity?

Danisco yogurt (now owned by DuPont)

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Phages are very bad for yogurt makers

Yogurt factory

Delivery of milk contaminated with phage could ruin the production of all yogurt!

For this reason, dairy scientists were interested in microbes with resistance to phage.

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Yogurt scientists hypothesized that CRISPR spacers were associated with immunity

2007 experiment:

  1. Challenge dairy bacterium Streptococcus thermophilus with lytic phages known to infect it
  2. Isolate resistant mutants that emerge
  3. Sequence their CRISPR loci

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Resistant strains acquired new spacers compared to WT

Ratio of plaques produced by strain to that of WT

S. thermophilus CRISPR locus

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Removing CRISPR sequences reduces immunity

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How widespread is CRISPR immunity?

CRISPR sequences have been found in:

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How do CRISPR-Cas complexes find the correct site amid all the DNA in the cell?

Millions of bases!

To answer this question, you must be able to watch CRISPR-Cas9 complexes bind to and move along DNA!

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DNA curtains enable measurement of single protein-DNA binding events

fluid flow

Objective

 

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DNA curtains facilitate TIRF imaging

Total internal reflection fluorescence

High refractive index (e.g. glass)

Low refractive index (e.g. water)

Light

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Total internal reflection fluorescence

Microscope glass

Aqueous buffer

  • Shine light beyond the critical angle
  • Create an exponentially decaying field
  • Illuminate only the fluorophores within ~100 nm of the cover glass
  • Facilitates single-molecule imaging!!

Fluorophores

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A quantum dot-labeled Cas9 enables single-molecule visualization

Cas9

quantum

dot

Fluorescent semiconductor nanoparticle

  • Extremely bright
  • Doesn’t photobleach

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A quantum dot-labeled Cas9 enables single-molecule visualization

DNA

Cas9

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Cas9-RNA complexes bind to DNA sequences determined by the RNA sequence

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Cas9 without guide RNA binds DNA, but not in a sequence-targeted way

Cas9

Cas9

+ RNA guide

- RNA guide

Does Cas9-RNA complex bind DNA and search along the DNA or does it diffuse in 3D, hopping on and off the DNA?

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Experiment to measure Cas9-RNA searching

Doubly-anchored DNA curtains with no flow

If Cas9-RNA complex binds to DNA and searches along it, you should see labeled complexes moving along DNA.

If instead complexes diffuse in 3D, hopping on and off DNA, you should see transient binding events at specific spots along the DNA.

 

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Cas9 complex hops on and off DNA

Single DNA molecule

 

CRISPR complex hops on and off DNA, binding transiently, except at target site, where it binds stably

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Cas9 complex hops on and off DNA

Time

Off-site binding times:

Why doesn’t the Cas9 complex cut the target DNA at these off sites?

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Both target complementarity and a PAM site are required for DNA interrogation and cutting

Experiment:

Modify this sequence

Detect products with a gel

Vary incubation time

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Both target complementarity and a PAM site are required for DNA interrogation and cutting

No PAM site results in no binding of Cas9!

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Proposed DNA search and cleave model

Note that this also accounts for why the CRISPR-Cas9 complex does not cut the bacterial genome: there is no PAM sequence!

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In summary

  1. Cells express cas genes and CRISPR RNAs
  2. Cas1-Cas2 complex recognizes PAM sequence and incorporates phage DNA into the bacterial CRISPR locus in such a way that the PAM sequence is not incorporated (!)
  3. When a Cas-RNA complex encounters DNA with the PAM sequence and the RNA target sequence adjacent to each other, it binds and cuts the DNA
  4. This acquired immunity can be passed down genetically to the next generation!

1

2

3

4

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Why has my father heard of CRISPR?

Doubled-stranded DNA

Protein-RNA complex

Cas9

Cas9

DNA with a double strand cut at a sequence determined by RNA-DNA base pairing!!!!

If you can just deliver the CRISPR-Cas9 complex to a cell nucleus, it will cut the genome at a specific location determined by the RNA sequence

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Before CRISPR-Cas9, sequence-specific DNA-binding proteins needed to be designed

  • Perfect sequence complementarity
  • Easily synthesized
  • Sequence complementarity may be difficult or impossible to design
  • Much off-target cutting

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What have we learned?

  • Bacteria (also archaea; sorry archaea) can acquire immunity to phages via CRISPR systems
  • CRISPR immunity is genetic and can be passed down to the next generation
  • CRISPR-Cas9 complex diffuses in 3D until it finds target DNA adjacent to PAM sequence
  • TIRF imaging allows single molecule observation of that process
  • This system can be leveraged for gene editing and many other biotechnology applications
    • Pretty much anything sequence-targeted!!!

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A takeaway from this semester

Everything we’ve talked about this semester is happening almost all the time in microbes and communities of microbes

And we’ve barely scratched the surface of what’s going on!!!