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Gene sharing in microbes: good for the individual,
good for the community?Rob Beiko
9 May 2014
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Image: Madeleine Price Ball, Wikimedia Commons
Griffith (1928) J Hygiene
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Microorganisms evolve in many different ways
Lateral gene transfer creates new opportunitiesby “reshuffling the deck”
Microorganisms interact in many different ways
What role does LGT play in building these interactions?
The short, short version
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Genome evolution in microbes
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Cummings et al. (2004) BMC Bioinformatics
RpoB mutations leading to rifampin resistance
U.S. NIAID
Mutation
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Gene loss
Lamelas et al. (2011) Appl Environ Microbiol
Seve
ral t
hous
and
gene
s
Cofactor synthesis, Amino acid synthesis, Carbohydrate degradation,…
Yurika Alexanderhttp://bugguide.net/node/view/510429
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Gene duplication
http://ultra.wikia.com/wiki/Godzilla
SignallingSecondary metabolitesSurface interaction proteinsHypotheticals
Schneiker et al. (2007) Nat Biotechnol
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2.bp.blogspot.com
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Holy moley!
Rinke et al., Nature (2013)
E
T
A
P
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AT
EP
AMPHORAWu and Eisen, Genome Biol (2008)
But wait!
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AMPHORA again!!Wu … Eisen, Nature (2009)
T
AE
P
But continueto wait!
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LATERAL GENE TRANSFER
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Aquifex aeolicus & friends
(Rob) Eveleigh et al., 2013
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Proteobacteria
Beiko, 2011
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P. aeruginosaP. fluorescensP. lePewtidaP. syringaeP. entomophilaP. stutzeriP. mendocina
(Catherine) Holloway and Beiko, 2010
“Plume”
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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…
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Smillie et al. (2011) Science
The Human Microbiome
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Bigthink.com
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Butyrate production – a crucialfunction, subject to LGT
All plausible “reference”species trees rejected!
(Conor) Meehan and Beiko (2014) Genome Biol Evol
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Larsbrink et al. (2014) Nature
Gunnarsson et al. (2006) Glycobiology
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Growth on xyloglucans
Red: YESBlue: NOGreen: MAYBE
Larsbrink et al. (2014) NatureDysgonomonas (termites!)
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W. Ford Doolittle, Sci Am (1999)
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Dagan et al. (2008) PNAS
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Winsor McCay (c.1920)www.loc.gov
(c) Sheri Amselwww.exploringnature.org
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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 Clements1874-1945“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 Gleason1882-1975
“species individualism”
botany.org
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A crucial role for interactionsASSEMBLAGEA collection of organisms, occupying the same place at the same time (observation)
COMMUNITYAn assemblage in which the organisms interact with one another in a non-neutral, non-trivial manner (hypothesis)
These definitions are controversial!
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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
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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)
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Periasamy and Kolenbrander (2009) J Bacteriol
Example: oral biofilm colonization
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The KB-1 communitya happy family
Duhamel and Edwards (2006) FEMS Microbiol EcolHug et al. (2012) BMC Genomics
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Mechanisms of Clostridium difficile suppressionby “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
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The dynamics of community formation
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Emergence of dependencies
Toxic substances
Nutrients
Boon, Meehan et al. (2013) FEMS Microbiol Rev
mBio (2012)
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The Distributed Genome Hypothesis
Why are costly LGT systems maintained?
Ehrlich et al. (2010) FEMS Immunol Med Microbiol
Killing your neighbors →→ release of free DNAUptake of DNA by survivors →→ increased diversity
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LGT, altruism and “public goods”
why give it away?
Product:DetoxificationResource scavengingetc
Conflict between host chromosome and mobile elementDistribution is preserved through LGT and mechanisms to kill cheaters
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LGT driving competition
Frigard et al. (2006) Nature
Photic zone
Subphotic zone
Rhodopsin-containing bacteria
Rhodopsin-lacking archaea
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Conclusions
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From assemblages to communities
• Gene loss and obligate associations
• Competition for resources due to LGT
• Signalling, sensing
• Strain-level distinctions matter!
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If interactions between microorganisms are mediated by the products of specific genetic traitsANDThe 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
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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!!
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FIN