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Lecture 24: Bacterial Biofilms Pt. II

Today:

  • Development of gene expression patterns in bacterial biofilms
  • How do biofilm cells resolve the problem of uneven nutrient distribution across the community?
  • How can biofilm cells engage in active communication to resolve this conflict?

membrane potential

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B. subtilis biofilm growth

agar substrate

objective

biofilm

MSgg media:

  • Glycerol (C)
  • Glutamate (N,C)
  • Salts (Ca, Fe, PO4, etc)

~1.3 cm by 60 hours

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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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A series of kinases in B. subtilis detects the environment and activates gene expression

KinD

KinC

KinB

KinA

Detect the extracellular environment

Detect the intracellular environment

inside cell

outside cell

cell envelope

Activate transcription factors

Leads to different cell states depending on conditions!

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Different conditions in time and space lead to different patterns of gene expression!

Not unlike development of a multicellular organism!

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B. subtilis cell types form developmental patterns!

Biofilm section:

Produce costly matrix for everyone

Can escape and form a biofilm somewhere else?

Can survive extreme conditions

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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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B. subtilis biofilm heterogeneity

Extracellular matrix

Motility

Spore

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There are many advantages to living in a biofilm community

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There are many advantages to living in a biofilm community

tobramycin (antibiotic)

Enhanced antibiotic tolerance!

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There are many advantages to living in a biofilm community

Matrix producer

Division of labor among differentiated cells!

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But there are also inevitable group conflicts!

The Ugly

The Bad

The Good

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Conflicts become even more complicated with large groups!

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How can the simplest organisms resolve group conflicts?

Bacillus subtilis

?

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Fundamental problem for cells in a biofilm

Biofilm

Competition for limited resources

glutamate

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Interior cells have limited nutrient access

… a global problem !

Nutrient

Nutrient access

glutamate

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Peripheral cells starve interior cells

Starvation

Growth

… a global problem !

Nutrient

Nutrient access

glutamate

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Interior

Periphery

Competition requires a collective solution

glutamate

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Long-range coordination

Interior

Periphery

Competition requires a collective solution

glutamate

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… diffusion limited

Interior

Periphery

Familiar bacterial mechanisms are insufficient

Quorum sensing molecule

glutamate

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Diffusion time increases non-linearly with distance!

Concentration also decays with diffusion!

Diffusion might not be the best way to couple behavior across a huge biofilm!

 

 

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Diffusion-limited signaling is insufficient

cells

distance

signal

amplitude

diffusion

interior

periphery

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An active relay mechanism?

distance

signal

amplitude

diffusion

interior

periphery

active relay

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Question: how is such long-range coordination possible?

nutrient access

interior

periphery

biofilm

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Action potentials enable long-range signaling

distance

signal

amplitude

diffusion

active relay

nervous system

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Action potentials are propagated by ion channels

nervous system

potassium channel

(Doyle, et al. (1998))

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Bacteria have ion channels . . .

nervous system

potassium channel

(Doyle, et al. (1998))

Courtesy of Steinar Stølen

B. subtilis Biofilm

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Bacteria generate action potentials!

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Bacteria generate action potentials!

objective

glass

PDMS

flow

Microfluidics

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Thioflavin-T

(membrane

potential)

Bacteria generate action potentials!

+

N

N

CH3

CH3

H3C

H3C

+

N

N

+

N

N

-

-

+

+

+

N

N

-

-

-

in

out

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Membrane potential

Bacteria generate action potentials!

Growth rate

Membrane potential

Thioflavin-T

(membrane

potential)

+

N

N

CH3

CH3

H3C

H3C

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Periodic pausing of biofilm growth

alleviates starvation of interior cells

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… which increases tolerance against antibiotics

Antibiotics

protected

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What is the mechanism?

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YugO

Mechanism for long-range signaling in biofilms

The trigger:

K+ ion channel

B. subtilis cell

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Glutamate limitation

for interior cells

cell

YugO

Mechanism for long-range signaling in biofilms

The trigger:

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Opening of YugO K+ channels

cell

YugO

Mechanism for long-range signaling in biofilms

The trigger:

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Mechanism for long-range signaling in biofilms

Signal relay:

YugO

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Depolarization of neighboring cells

YugO

Mechanism for long-range signaling in biofilms

Signal relay:

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Reduced glutamate uptake

GltP

YugO

Mechanism for long-range signaling in biofilms

Signal relay:

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Glutamate limitation

YugO

Mechanism for long-range signaling in biofilms

Signal relay:

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Opening of YugO channels

YugO

Mechanism for long-range signaling in biofilms

Signal relay:

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Bacteria propagate action potentials!?

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Active long-range signal propagation

Diffusion

Signal amplitude

Active relay

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Electrical signaling enables nutrient time-sharing!

nutrient access

periodic growth

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Liu, et al. (2017)

Electrical signaling can couple distant biofilms

Liu, et al. (2017)

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Electrical signaling can attract motile cells!

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What have we learned?

  • Bacterial biofilms generate heterogeneous patterns of cell types, not unlike developing multicellular organisms�
  • Biofilms can resolve intra-community conflicts such as nutrient competition�
  • Biofilms can engage in electrochemical cell-to-cell signaling!!