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Lecture 23: Biofilms

Today:

  • How do bacterial grow on surfaces?
    • Biofilms
  • What are biofilms?
  • How is the biofilm state different from the liquid culture state?
  • What are the benefits of living in a biofilm as opposed to on your own?
    • Antibiotic tolerance
    • Division of labor

Disclaimer: very little is known about biofilms. Not everything in this lecture necessarily applies very widely!

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What is the environment of the microbes we’ve studied so far?

Liquid Culture

Gel Pads

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What are the key features of these laboratory environments?

Often very nutrient-rich

Often little spatial structure

Often strains bred for growth on these substrates (more on this later)

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What are features of the natural microbial environment?

Not always rich nutrient availability

~50 mM dissolved carbon

~40-60 µM dissolved carbon

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What are features of the natural microbial environment?

Intricate spatial surface structure

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In the wild, a huge fraction of microbial biomass is associated with surfaces!

plant root

10 µm

bacteria

25 µm

chitin particle

These surface-attached communities are called biofilms!

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What is a biofilm?

  1. Microbial cells stuck together by a polymer matrix����
  2. Microbial cells stuck together by a polymer matrix with 3D morphology��
  3. Multiple species of microbes stuck together in a 3D structure

100 µm

Species 1

Species 2

Warning: a lot of bickering, challenges in manuscript review!

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B. subtilis biofilm growth

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Where are biofilms? Everywhere.

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Biofilms are notorious for forming on medical devices and liquid processing systems

Biofilm-forming strain of opportunistic pathogen Pseudamonas Aeruginosa

Flow-cell with dimensions of a medical device, e.g. catheter

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Biofilms are thought to represent a major evolutionary transition toward multicellularity

Often called “planktonic” cells

Often called “biofilms”, “plaques”, etc

  • Creates new, microbe-engineered habitats > new opportunities
  • Protects cells from loss of nutrients, chemical attacks, predators
  • Facilitates division of labor

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-James Shapiro,

Scientific American (1988)

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The biofilm life cycle

(image courtesy of George O’Toole, Dartmouth)

1. Swimming cells find a surface

2. Cells adhere to the surface and secrete extracellular matrix

3. Cells form an attached colony

4. Cells form a mature biofilm

5. Motile cells disperse from the biofilm to potentially form a new one elsewhere

Decent amount of research here.

Not much here.

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What is a biofilm vs a mere colony?

“Colony”:

  • Smooth
  • Composed of mostly homogeneous cells (similar profiles of gene expression)
  • “domesticated” strains and/or richly nutritious media

“Biofilm”:

  • Highly, structured, multiscale 3D organization
  • Highly heterogeneous cells (different gene expression profiles in different places; like anatomy of an organism!)
  • “undomesticated”/wild strains

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Domesticated colony: little spatial structure

Smooth colony-scale structure

Some cell-scale structure

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Undomesticated “biofilm” of B. subtilis

Credit to Michael Zulch

Emergent structure over many scales

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Domestication

1890s E. coli isolate

Nutrient-rich broth

Cell-dense culture

Nutrient-rich broth

Cell-dense culture

X10,000

1990s E. coli “lab strain”

This process selects for mutants that grow quickly in the nutrient-rich conditions.

Many behaviors quickly disappear in the domestication process, notably biofilm formation.

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Earliest biofilm experiments: how does the presence of a surface impact bacterial growth?

2 bacterial cultures:

  • Media with glucose and peptone (various polypeptides)
  • One culture contains only media
  • The other also contains mm-sized glass beads

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How does the presence of a surface impact bacterial growth?

2 bacterial cultures:

  1. Inoculate with E. coli
  2. Grow for 72 hours without agitation
  3. Take a small volume and spread on plate
  4. Count colonies of plate after 48 hours at 37 °C
  5. Repeat for several nutrient concentrations

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Let’s quickly plot the data in python!

Open up jupyter

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How does the presence of a surface impact bacterial growth?

At “high” nutrient concentration, maybe not at all?

At low nutrient concentration, potentially a lot!

Already ~100x less than standard growth medium

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How do biofilms form?

Potentially through a sense of touch! Experiment:

outlet/cell waste

inlet

flow cell 1 (FC1)

flow cell 2 (FC2)

  1. Flow in P. aeruginosa cells into FC1 with FC2 closed off
  2. Observe cells encounter glass coverslip and measure residence time on the surface
  3. After many hours, unseal FC2 to let cells into FC2
  4. For each cell that sticks to the glass, measure how long they have been in the chamber before sticking, and how many generations of cells stick to the surface

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How do biofilms form?

Potentially through a sense of touch!

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How do biofilms form?

Potentially through a sense of touch!

Surface-exposed cells, when exposed to a new surface, stick to it more quickly than cells that have not been exposed to a surface.

FC1 cells

FC2 cells

Time since introduction into chamber

Each dot represents one cell that stuck to glass for at least 15 minutes

“Surface-naïve” cells take hours to stick to the glass surface

Surface-exposed cells start to stick immediately

(Ignore y-axes for now)

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How do biofilms form?

Surface-exposed cells stick to surfaces for more generations than surface-naïve cells

FC1 cells

FC2 cells

Parent sticky cells

Example family trees of cells that stick to the glass

Cells that detach and swim away

Many generations of cells that stick. There is a memory of encountering the surface that facilitates multiple generations sticking and growing on the surface

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How do biofilms form?

Surface exposure triggers intracellular cyclic AMP signaling that engages biofilm genes. Perform the experiment with a fluorescent reporter for cAMP activity

Mutant strain with high cAMP levels

cAMP level

Growth on surface

# generations on surface

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How do biofilms form?

Surface sensing and cAMP levels are associated with extracellular pili that encounter the surface!

Type-IV Pilus

P. aeruginosa plausibly touching surfaces with a pilus, activating cAMP signaling sticking to surface, and forming a biofilm!

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What are the benefits to being in a biofilm?

We will cover two:

  1. Enhanced antibiotic tolerance�
  2. Division of labor via cell differentiation

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Biofilms are notably more resistant to antibiotics than planktonic cells

medical device, e.g. catheter

fluid flow

Experiment 1

Experiment 2

  1. Flow planktonic cells through device
  2. Incubate with antibiotics
  3. Spread resulting culture on petri dish
  4. Count relative number of colonies formed compared to no antibiotics

Same as above but with biofilm.

Planktonic cells dead after 50 µg/ml

Biofilm cells still viable at 1000 µg/ml

“20 times more tolerant of antibiotics”.

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Anti-biotic tolerance is not due merely to the inability of antibiotics to penetrate the matrix

P. Aeruginosa strains:

Phase

Membrane stain

Forms normal biofilms

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45E7 strain forms robust biofilms indistinguishable from WT, but is killed easily by antibiotics

After tobramycin treatment:

Phase

Cell viability stain

Cell death stain

The ability to secrete matrix and form a biofilm is not sufficient to tolerate antibiotics. Tolerance is conferred by distinct phenotypic states that arise in biofilms or emergent properties!

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Biofilm cells divide labor by taking up different phenotypic states

B. subtilis can differentiate into different cell states, much like a developing organism!

Can swim

Can secrete matrix to form biofilm

Become dormant to survive extreme conditions

Can take up DNA

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B. subtilis cell types form developmental patterns!

Biofilm section:

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B. subtilis cell types form developmental patterns!

Extracellular matrix

Motility

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B. subtilis biofilm heterogeneity

Extracellular matrix

Spore

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B. subtilis biofilm heterogeneity

Extracellular matrix

Motility

Spore

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What have we learned?

  • Bacteria in many (most?) environments live adhered to surfaces as biofilms
  • The surface-adhered state can allow superior growth and survival under low-nutrient conditions
  • Biofilms may form by motile cells physically sensing a surface
  • Biofilms can be highly tolerant of antibiotics
  • Biofilms generate heterogeneous patterns of cell types in a process reminiscent of development