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.
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
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…
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!)
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)
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
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
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!!
