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Gene sharing in microbes:
good for the individual,
good for the community?
Rob Beiko
9 May 2014
Image: Madeleine Price Ball, Wikimedia Commons
Griffith (1928) J Hygiene
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
Genome evolution in microbes
Cummings et al. (2004) BMC Bioinformatics
RpoB mutations leading to rifampin resistance
U.S. NIAID
Mutation
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
Gene
duplication
http://ultra.wikia.com/wiki/Godzilla
Signalling
Secondary metabolites
Surface interaction proteins
Hypotheticals
Schneiker et al. (2007) Nat Biotechnol
2.bp.blogspot.com
Holy
moley!
Rinke et al., Nature (2013)
E
T
A
P
A
T
E
P
AMPHORA
Wu and Eisen, Genome Biol (2008)
But wait!
AMPHORA again!!
Wu … Eisen, Nature (2009)
T
A
E
P
But continue
to wait!
LATERAL GENE TRANSFER
Aquifex aeolicus & friends
(Rob) Eveleigh et al., 2013
Proteobacteria
Beiko, 2011
P. aeruginosa
P. fluorescens
P. lePewtida
P. syringae
P. entomophila
P. stutzeri
P. mendocina
(Catherine) Holloway and Beiko, 2010
“Plume”
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…
Smillie et al. (2011) Science
The Human
Microbiome
Bigthink.com
Butyrate production – a crucial
function, subject to LGT
All plausible “reference”
species trees rejected!
(Conor) Meehan and Beiko (2014) Genome Biol Evol
Larsbrink et al. (2014) Nature
Gunnarsson et al. (2006) Glycobiology
Growth on xyloglucans
Red: YES
Blue: NO
Green: MAYBE
Larsbrink et al. (2014) Nature
Dysgonomonas (termites!)
W. Ford Doolittle, Sci Am (1999)
Dagan et al. (2008) PNAS
Gene sharing in microbes: good for the individual, good for the community?
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
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!
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
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)
Periasamy and Kolenbrander (2009) J Bacteriol
Example: oral biofilm colonization


The KB-1 community
a happy family
Duhamel and Edwards (2006) FEMS Microbiol Ecol
Hug et al. (2012) BMC Genomics
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
The dynamics of community
formation
Emergence of dependencies
Toxic substances
Nutrients
Boon, Meehan et al. (2013) FEMS Microbiol Rev
mBio (2012)
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
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
LGT driving competition
Frigard et al. (2006) Nature
Photic zone
Subphotic zone
Rhodopsin-containing bacteria
Rhodopsin-lacking archaea
Conclusions
From assemblages to
communities
• Gene loss and obligate associations
• Competition for resources due to LGT
• Signalling, sensing
• Strain-level distinctions matter!
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
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!!
FIN

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Gene sharing in microbes: good for the individual, good for 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
  • 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
  • 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!
  • 13. Aquifex aeolicus & friends (Rob) Eveleigh et al., 2013
  • 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
  • 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
  • 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