Social interactions and cheating in the microbial world

Steve AllisonUC Irvine

Ecology and Evolutionary BiologyEarth System Science

allisons@uci.edu

What is a microbe?

• Bacteria, fungi, and protists• Interact with environment at microscopic

scales

NIH David Read

Microbes are diverse and abundant

• 1 billion bacteria in a handful of soil

• 1 million in a mouthful of seawater

• More biomass than in plants• 10 bacterial cells for every 1

human cell in your body• 1-10 million species of

microbes globally

Whitman et al. 1998, Norm Pace

Why microbes are important

• Global carbon cycling• Nutrient cycling, soil fertility (agriculture)• Biomolecules; drug discovery

Microbe “social lives”

• Many microbes live in complex communities• They need energy and nutrients• Microbial behaviors:

Cooperation Communication Cheating

• Behaviors require production of chemicals that operate outside the cell

Cooperation example: Biofilms

Polysaccharides

Where are biofilms?

• On your teeth• Inside showerheads• On rocks in streams• Between particles of soil• Almost anywhere with liquid water

Communication: Quorum sensing

• A behavior is triggered when cell densities cross a threshold

• Requires production of an inducer molecule

InducerProduct

High densityLow density

Reasons for quorum sensing• Coordination of group behavior• Evasion of host defenses by pathogen• Can trigger biofilm formation (or cessation)

Costs and benefits of cooperationNutrientsOxygen

Polysaccharides

Evolution of cheating

• Making biofilm is expensive• All microbes benefit• Natural selection favors cheater mutants

Paul Rainey

Cheaters

Do cheaters win?

• What might prevent cheaters from taking over? Producers must get a bigger share of the benefits Products benefit close relatives, not cheaters (kin

selection) Spatial structure

Spatial structure favors producers

Chuang et al. 2009

BottleneckCheater

Producer

Extracellular enzymes

• Some microbes “forage” with enzymes• They eat complex chemicals produced by

plants, animals, and other microbes• Prevents the world from filling with dead

bodies• Enzymes contain carbon and nitrogen

Enzyme model

CheaterProducer

Processes:

•Metabolism

•Reproduction

Substrate Enzyme Product

•Enzyme synthesis

•Diffusion•Enzyme catalysis

•Input

•Product uptake

Allison 2005

Coexistence at low diffusion

Increasing enzyme diffusion

Pop

ulat

ion

size Cheater

Producer

Time

Cheaper enzym

esP

opul

atio

n si

ze

T im e

Increasing enzyme diffusion

Pop

ulat

ion

size Cheater

Producer

Time

Cheating reduces enzyme function

Low product formation

Product concentration(mg/l)

Cheater experiments

• Pseudomonas fluorescens• Producer: degrades

protein with protease• Cheater: protease

knockout

• Well mixed flasks• Protein medium• Digested protein medium

Collaborators: Mindy Ta, Lucy Lu, Jennifer Chen

Cheaters suppress producers on protein

0 20 40 60 80

0.0

0.2

0.4

0.6

0.8

1.0

1.2

Time (h)

Op

tic

al

De

ns

ity

Protein

Producers

Cheaters

Competition

Cheaters suppress producers on protein

0 20 40 60 80

0.0

0.2

0.4

0.6

0.8

1.0

1.2

Time (h)

Op

tic

al

De

ns

ity

0 20 40 60 80

0.0

0.5

1.0

1.5

Time (h)

Op

tic

al

De

ns

ity

Protein Digested protein

Producers

Cheaters

Competition

Cheaters suppress protease production

0 10 20 30 40 50 60 70

0.0

0.2

0.4

0.6

0.8

Time (h)

Ac

tiv

ity

(m

g/m

l/h

)

Protein

Producers

Cheaters

Competition

Role of enzymes in the ocean

WHOI

MICRO time seriesNewport Beach, CA

Marine snow

Collaborators: Adam Martiny, Sunny Jiang, numerous undergrads

Most peptidase activity is bound

0

100

200

300

400

500

600L

AP

Ac

tiv

ity

(m

icro

mo

l/L

/h)

Jan Feb Mar Apr May Jun Jul Aug Sep

<0.2 micron<2.7 micronUnfiltered

0

50

100

150

PH

OS

Ac

tiv

ity

(m

icro

mo

l/L

/h)

Jan Feb Mar Apr May Jun Jul Aug Sep

<0.2 micron<2.7 micronUnfiltered

Phosphatase is freely dissolved

Ocean carbon sequestration

CO2, Nutrients

CO2

Phytoplankton

Surface ocean

Deep ocean

Cheater

Producer

Take-home messages

• Microbes are diverse and important• Microbes cooperate, but natural selection can

favor cheating• Microbial behavior and evolution has

consequences for ecosystems

• Thank you: Lab members, NSF, audience