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 opportunitiesby “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

Seve

ral t

hous

and

gene

s

Cofactor synthesis, Amino acid synthesis, Carbohydrate degradation,…

Yurika Alexanderhttp://bugguide.net/node/view/510429

Gene duplication

http://ultra.wikia.com/wiki/Godzilla

SignallingSecondary metabolitesSurface interaction proteinsHypotheticals

Schneiker et al. (2007) Nat Biotechnol

2.bp.blogspot.com

Holy moley!

Rinke et al., Nature (2013)

E

T

A

P

AT

EP

AMPHORAWu and Eisen, Genome Biol (2008)

But wait!

AMPHORA again!!Wu … Eisen, Nature (2009)

T

AE

P

But continueto wait!

LATERAL GENE TRANSFER

Aquifex aeolicus & friends

(Rob) Eveleigh et al., 2013

Proteobacteria

Beiko, 2011

P. aeruginosaP. fluorescensP. lePewtidaP. syringaeP. entomophilaP. stutzeriP. 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 crucialfunction, 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: YESBlue: NOGreen: MAYBE

Larsbrink et al. (2014) NatureDysgonomonas (termites!)

W. Ford Doolittle, Sci Am (1999)

Dagan et al. (2008) PNAS

Winsor McCay (c.1920)www.loc.gov

(c) Sheri Amselwww.exploringnature.org

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

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!

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 communitya happy family

Duhamel and Edwards (2006) FEMS Microbiol EcolHug et al. (2012) BMC Genomics

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

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 DNAUptake of DNA by survivors →→ increased diversity

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

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 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

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