1. Social interactions and cheating in the microbial world
Steve Allison
UC Irvine
Ecology and Evolutionary Biology
Earth System Science

2. What is a microbe? Bacteria, fungi, and protists
Interact with environment at microscopic scales
NIH
David Read

3. 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

4. Why microbes are important
Global carbon cycling
Nutrient cycling, soil fertility (agriculture)
Biomolecules; drug discovery

5. 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

6. Cooperation example: Biofilms
Polysaccharides

7. Where are biofilms? On your teeth Inside showerheads
On rocks in streams
Between particles of soil
Almost anywhere with liquid water

8. Communication: Quorum sensing
A behavior is triggered when cell densities cross a threshold
Requires production of an inducer molecule
Inducer
Product
Low density
High density

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

10. Costs and benefits of cooperation
Nutrients
Oxygen
Polysaccharides

11. Evolution of cheating Making biofilm is expensive All microbes benefit
Natural selection favors cheater mutants
Cheaters
Paul Rainey

12. 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

13. Spatial structure favors producers
Cheater
Bottleneck
Producer
Chuang et al. 2009

14. 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

15. Enzyme model Processes: Metabolism Reproduction Input Enzyme synthesis
Substrate
Enzyme
Product
Cheater
Producer
Processes:
Metabolism
Reproduction
Input
Enzyme synthesis
Diffusion
Enzyme catalysis
Enzymes are a public good
Product uptake
Allison 2005

16. Coexistence at low diffusion
Increasing enzyme diffusion
Time

17. Increasing enzyme diffusion
Time
Cheaper enzymes

18. Cheating reduces enzyme function
Product concentration
(mg/l)
Low product formation

19. 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

20. Cheaters suppress producers on protein
Competition
Cheaters
Other plate counts show cheaters do equally well or better when producers present, while producers do worse when cheaters present.

21. Cheaters suppress producers on protein
Digested protein
Producers
Competition
Cheaters
Other plate counts show cheaters do equally well or better when producers present, while producers do worse when cheaters present.

22. Cheaters suppress protease production
Protein
Producers
Time interaction also significant
Competition
Cheaters

23. Role of enzymes in the ocean
MICRO time series
Newport Beach, CA
Collaborators: Adam Martiny, Sunny Jiang, numerous undergrads
WHOI
Marine snow

24. Most peptidase activity is bound

25. Phosphatase is freely dissolved

26. Ocean carbon sequestration
CO2
CO2, Nutrients
Phytoplankton
Cheater
Producer
Surface ocean
Deep ocean

27. 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