1) Gene sharing between microbes, called lateral gene transfer (LGT), plays an important role in building interactions between microorganisms. LGT allows for the reshuffling of genes which creates new opportunities. 2) Successful gene acquisitions through LGT often reflect shared environments between lineages, such as high-temperature or high-acidity habitats. This suggests gene sharing occurs preferentially between microbes in similar ecological niches. 3) Microbial communities may be considered as an "ecology of genes" rather than just organisms, since interactions between microbes are often mediated by specific genetic traits which are readily laterally transferred between members of the community.

1. Gene sharing in microbes:
good for the individual,
good for the community?
Rob Beiko
9 May 2014

2. Image: Madeleine Price Ball, Wikimedia Commons
Griffith (1928) J Hygiene

3. Microorganisms evolve in many different ways
Lateral gene transfer creates new opportunities
by “reshuffling the deck”
Microorganisms interact in many different ways
What role does LGT play in building these interactions?
The short, short version

4. Genome evolution in microbes

5. Cummings et al. (2004) BMC Bioinformatics
RpoB mutations leading to rifampin resistance
U.S. NIAID
Mutation

6. Gene
loss
Lamelas et al. (2011) Appl Environ Microbiol
Severalthousandgenes
Cofactor synthesis, Amino acid synthesis, Carbohydrate degradation,…
Yurika Alexander
http://bugguide.net/node/view/510429

7. Gene
duplication
http://ultra.wikia.com/wiki/Godzilla
Signalling
Secondary metabolites
Surface interaction proteins
Hypotheticals
Schneiker et al. (2007) Nat Biotechnol

8. 2.bp.blogspot.com

9. Holy
moley!
Rinke et al., Nature (2013)
E
T
A
P

10. A
T
E
P
AMPHORA
Wu and Eisen, Genome Biol (2008)
But wait!

11. AMPHORA again!!
Wu … Eisen, Nature (2009)
T
A
E
P
But continue
to wait!

12. LATERAL GENE TRANSFER

13. Aquifex aeolicus & friends
(Rob) Eveleigh et al., 2013

14. Proteobacteria
Beiko, 2011

15. P. aeruginosa
P. fluorescens
P. lePewtida
P. syringae
P. entomophila
P. stutzeri
P. mendocina
(Catherine) Holloway and Beiko, 2010
“Plume”

16. Highways of gene sharing:
Beiko et al. (2005)
Gene sharing occurs preferentially between lineages
Successful gene acquisitions often reflect shared
environments (such as high-temperature or high-acidity
habitats)
AND…

17. Smillie et al. (2011) Science
The Human
Microbiome

18. Bigthink.com

19. Butyrate production – a crucial
function, subject to LGT
All plausible “reference”
species trees rejected!
(Conor) Meehan and Beiko (2014) Genome Biol Evol

20. Larsbrink et al. (2014) Nature
Gunnarsson et al. (2006) Glycobiology

21. Growth on xyloglucans
Red: YES
Blue: NO
Green: MAYBE
Larsbrink et al. (2014) Nature
Dysgonomonas (termites!)

22. W. Ford Doolittle, Sci Am (1999)

23. Dagan et al. (2008) PNAS

25. Theory of ecological succession: progression of states to a “climax”, similar to the
development of a living organism
“The author [i.e., Clements] considers physiology and ecology as essentially the
same…”
Bessey, review of “Plant Physiology and Ecology”, Science (1907)
Frederic Clements
1874-1945
“climax states”
people.wku.edu
Crucial roles for randomness, precedence, spatial scale – ecology is being held back
by attempts to identify and classify “climax communities”
"for ten years or thereabout, I was an ecological outlaw, sometimes referred to as ‘a
good man gone wrong.' “ (1953)
“Gleason observed that removal of one association would allow the expansion of the
other, suggesting that the control of the environment by organisms was, in fact,
limiting the spread of an association.”
McIntosh, obituary, Bull Torrey Botanical Club (1975)
Henry Gleason
1882-1975
“species individualism”
botany.org

26. A crucial role for interactions
ASSEMBLAGE
A collection of organisms, occupying the same place
at the same time (observation)
COMMUNITY
An assemblage in which the organisms interact with
one another in a non-neutral, non-trivial manner
(hypothesis)
These definitions are controversial!

27. Example: mouse feces
(because why not)
Some Clostridiales
“Genus”-level classifications
Various Lachnospiraceae
Bacteroidales family S24-7 (??)
Ruminococcaceae of some kind
Ruminococcaceae of some other kind
Also Lachnospiraceae

28. Community
Assemblage
Could manifest as:
• Subsets of the assemblage participating in interactions
• Asymmetric dependencies among microorganisms
• Conditional dependencies
(e.g., the synergen hypothesis: Mike Surette, McMaster)

29. Periasamy and Kolenbrander (2009) J Bacteriol
Example: oral biofilm colonization



30. The KB-1 community
a happy family
Duhamel and Edwards (2006) FEMS Microbiol Ecol
Hug et al. (2012) BMC Genomics

31. Mechanisms of Clostridium difficile suppression
by “healthy” host microbiota
• Short-chain fatty acid production (maybe)
• Cleaving C. diff toxins
• Colonization inhibition
• Consuming host sugars
C. difficile fights back by inducing inflammation
A less happy family:
Clostridium difficile, your gut
microbes, and you

32. The dynamics of community
formation

33. Emergence of dependencies
Toxic substances
Nutrients
Boon, Meehan et al. (2013) FEMS Microbiol Rev
mBio (2012)

34. The Distributed Genome Hypothesis
Why are costly LGT systems maintained?
Ehrlich et al. (2010) FEMS Immunol Med Microbiol
Killing your neighbors →→ release of free DNA
Uptake of DNA by survivors →→ increased diversity

35. LGT, altruism and “public goods”
why give it away?
Product:
Detoxification
Resource scavenging
etc
Conflict between host chromosome and mobile element
Distribution is preserved through LGT and mechanisms to kill cheaters

36. LGT driving competition
Frigard et al. (2006) Nature
Photic zone
Subphotic zone
Rhodopsin-containing bacteria
Rhodopsin-lacking archaea

37. Conclusions

38. From assemblages to
communities
• Gene loss and obligate associations
• Competition for resources due to LGT
• Signalling, sensing
• Strain-level distinctions matter!

39. If interactions between microorganisms are
mediated by the products of specific genetic traits
AND
The genes that underlie these traits are readily
transferred
Does this mean that we should consider microbial
ecology as an ecology of genes, rather than
organisms?
Boon, Meehan et al. (2013) FEMS Microbiol Rev

40. How do we investigate this?
• Metagenomics?
+ abundance information
- difficult to determine “who is doing what”
• Pure culture?
+ CAN determine “who is doing what”
- culture conditions do not mimic in vivo setting, functions
could be rapidly lost or altered
- lose strain-level diversity
• Mixed culture?
+ keep strain-level diversity, maybe
- back to the metagenomics problem!!

41. FIN