a phylogeny driven genomic encyclopedia of bacteria and archaea

A phylogeny driven genomic encyclopedia of bacteria and archaea

Jonathan A. Eisen

Talk at Stanford UniversityApril 17, 2010

Saturday, April 24, 2010

Bacterial evolve


Fleischmann et al. 1995


Microbial genomes

From http://genomesonline.orgSaturday, April 24, 2010

rRNA Tree of Life

Based on tree by

Norm Pace


The Tree is not Happy

Based on tree by

Norm Pace


Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi

FirmicutesFusobacteria Actinobacteria

Cyanobacteria

Chlamydia

Spriochaetes

Deinococcus-Thermus Aquificae

Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira

SynergistesDeferribacteres

Thermudesulfobacteria

Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter

• At least 40 phyla of bacteria

As of 2002

Based on Hugenholtz, 2002


Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter


• Genome sequences are mostly from three phyla

As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter



• Some other phyla are only sparsely sampled

As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter




• Same trend in Archaea

As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter




• Same trend in Eukaryotes

As of 2002



Filling in the Genomic Phylogenetic Gaps

• Common approach within some eukaryotic groups

• Many small projects funded to fill in some bacterial or archaeal gaps

• Phylogenetic gaps in bacterial and archaeal projects commonly lamented in literature


Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter




• Solution I: sequence more phyla

• NSF-funded Tree of Life Project

• A genome from each of eight phyla

Eisen & Ward, PIs


Phylum

Species selected

Chrysiogenes

Chrysiogenes arsenatis (GCA)

Coprothermobacter

Coprothermobacter proteolyticus (GCBP)

Dictyoglomi

Dictyoglomus thermophilum (GD T )

Thermodesulfobacteria

Thermodesulfobacterium commune (GTC)

Nitrospirae

Thermodesulfovibrio yellowstonii (GTY)

Thermomicrobia

Thermomicrobium roseum (GTR )

Deferribacteres

Geovibrio thiophilus (GGT)

Synergistes

Synergistes jonesii (GSJ)

Organisms Selected


Bacterial aTOL Project AIMS

• Improve resolution of deep branches in the bacterial tree

• Launch biological studies of these phyla

• Leverage data for interpreting environmental surveys


T. roseum genome


From http://genomesonline.org

Microbial genomes


The Tree of Life is Still Angry


Major Lineages of Actinobacteria2.5.1 Acidimicrobidae2.5.1.1 Unclassified2.5.1.2 "Microthrixineae2.5.1.3 Acidimicrobineae2.5.1.4 BD2-102.5.1.5 EB10172.5.2 Actinobacteridae2.5.2.1 Unclassified2.5.2.10 Ellin306/WR1602.5.2.11 Ellin50122.5.2.12 Ellin50342.5.2.13 Frankineae2.5.2.14 Glycomyces2.5.2.15 Intrasporangiaceae2.5.2.16 Kineosporiaceae2.5.2.17 Microbacteriaceae2.5.2.18 Micrococcaceae2.5.2.19 Micromonosporaceae2.5.2.2 Actinomyces2.5.2.20 Propionibacterineae2.5.2.21 Pseudonocardiaceae2.5.2.22 Streptomycineae2.5.2.23 Streptosporangineae2.5.2.3 Actinomycineae2.5.2.4 Actinosynnemataceae2.5.2.5 Bifidobacteriaceae2.5.2.6 Brevibacteriaceae2.5.2.7 Cellulomonadaceae2.5.2.8 Corynebacterineae2.5.2.9 Dermabacteraceae2.5.3 Coriobacteridae2.5.3.1 Unclassified2.5.3.2 Atopobiales2.5.3.3 Coriobacteriales2.5.3.4 Eggerthellales2.5.4 OPB412.5.5 PK12.5.6 Rubrobacteridae2.5.6.1 Unclassified2.5.6.2 "Thermoleiphilaceae2.5.6.3 MC472.5.6.4 Rubrobacteraceae

2.5 Actinobacteria2.5.1 Acidimicrobidae2.5.1.1 Unclassified2.5.1.2 "Microthrixineae2.5.1.3 Acidimicrobineae2.5.1.3.1 Unclassified2.5.1.3.2 Acidimicrobiaceae2.5.1.4 BD2-102.5.1.5 EB10172.5.2 Actinobacteridae2.5.2.1 Unclassified2.5.2.10 Ellin306/WR1602.5.2.11 Ellin50122.5.2.12 Ellin50342.5.2.13 Frankineae2.5.2.13.1 Unclassified2.5.2.13.2 Acidothermaceae2.5.2.13.3 Ellin60902.5.2.13.4 Frankiaceae2.5.2.13.5 Geodermatophilaceae2.5.2.13.6 Microsphaeraceae2.5.2.13.7 Sporichthyaceae2.5.2.14 Glycomyces2.5.2.15 Intrasporangiaceae2.5.2.15.1 Unclassified2.5.2.15.2 Dermacoccus2.5.2.15.3 Intrasporangiaceae2.5.2.16 Kineosporiaceae2.5.2.17 Microbacteriaceae2.5.2.17.1 Unclassified2.5.2.17.2 Agrococcus2.5.2.17.3 Agromyces2.5.2.18 Micrococcaceae2.5.2.19 Micromonosporaceae2.5.2.2 Actinomyces2.5.2.20 Propionibacterineae2.5.2.20.1 Unclassified2.5.2.20.2 Kribbella2.5.2.20.3 Nocardioidaceae2.5.2.20.4 Propionibacteriaceae2.5.2.21 Pseudonocardiaceae2.5.2.22 Streptomycineae2.5.2.22.1 Unclassified2.5.2.22.2 Kitasatospora2.5.2.22.3 Streptacidiphilus2.5.2.23 Streptosporangineae2.5.2.23.1 Unclassified2.5.2.23.2 Ellin51292.5.2.23.3 Nocardiopsaceae2.5.2.23.4 Streptosporangiaceae2.5.2.23.5 Thermomonosporaceae2.5.2.3 Actinomycineae2.5.2.4 Actinosynnemataceae2.5.2.5 Bifidobacteriaceae2.5.2.6 Brevibacteriaceae2.5.2.7 Cellulomonadaceae2.5.2.8 Corynebacterineae2.5.2.8.1 Unclassified2.5.2.8.2 Corynebacteriaceae2.5.2.8.3 Dietziaceae2.5.2.8.4 Gordoniaceae2.5.2.8.5 Mycobacteriaceae2.5.2.8.6 Rhodococcus2.5.2.8.7 Rhodococcus2.5.2.8.8 Rhodococcus2.5.2.9 Dermabacteraceae2.5.2.9.1 Unclassified2.5.2.9.2 Brachybacterium2.5.2.9.3 Dermabacter2.5.3 Coriobacteridae2.5.3.1 Unclassified2.5.3.2 Atopobiales2.5.3.3 Coriobacteriales2.5.3.4 Eggerthellales2.5.4 OPB412.5.5 PK12.5.6 Rubrobacteridae2.5.6.1 Unclassified2.5.6.2 "Thermoleiphilaceae2.5.6.2.1 Unclassified2.5.6.2.2 Conexibacter2.5.6.2.3 XGE5142.5.6.3 MC472.5.6.4 Rubrobacteraceae


Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter



• Most phyla with cultured species are sparsely sampled

• Lineages with no cultured taxa even more poorly sampled

• Solution - use tree to really fill gaps

Well sampled phyla


http://www.jgi.doe.gov/programs/GEBA/pilot.htmlSaturday, April 24, 2010

GEBA Pilot Project Overview

• Identify major branches in rRNA tree for which no genomes are available

• Identify a cultured representative for each group

• Grow > 200 of these and prep. DNA• Sequence and finish 100• Annotate, analyze, release data• Assess benefits of tree guided sequencing


GEBA Pilot Target List

0

5

10

15

20

25

30

35

B: A

ctinob

acteria

(High GC)

B: A

minan

aero

bia

B: A

quifica

e

B: B

actero

idetes

B: C

hlor

oflexi

B: D

efer

ribac

tere

s

B: D

efer

ribac

tere

s

B: D

eino

cocc

i

B: D

elta Pro

teob

acteria

B: Eps

ilon Pr

oteo

bacter

ia

B: Firm

icutes

B: Fus

obac

teria

B: G

amma Pr

oteo

bacter

ia

B: G

emmatim

onad

etes

B: H

aloa

naer

obiales

B: Planc

tomyc

etes

B: S

piro

chae

tes

B: The

rmod

esulfoba

cter

ia

B: The

rmod

esulfobia

B: The

rmov

enab

ulae

A: H

alob

acteria

A: A

rcha

eoglob

i

A: M

etha

noba

cter

ia

A: M

etha

nomicr

obia

A: The

rmoc

occi

A: The

rmop

rotei

Phyla

# o

f G

en

om

es


Why Increase Taxonomic Coverage?

• Gene discovery• Annotation, functional prediction• Metagenomic analysis• Mechanisms of diversification• Species phylogeny and classification


GEBA Pilot Project: Components• Project overview (Phil Hugenholtz, Nikos Kyrpides, Jonathan

Eisen, Eddy Rubin, Jim Bristow)• Project management (David Bruce, Eileen Dalin, Lynne Goodwin)• Culture collection and DNA prep (DSMZ, Hans-Peter Klenk)• Sequencing and closure (Eileen Dalin, Susan Lucas, Alla Lapidus,

Mat Nolan, Alex Copeland, Cliff Han, Feng Chen, Jan-Fang Cheng)• Annotation and data release (Nikos Kyrpides, Victor Markowitz, et

al)• Analysis (Dongying Wu, Kostas Mavrommatis, Martin Wu, Victor

Kunin, Neil Rawlings, Ian Paulsen, Patrick Chain, Patrik D’Haeseleer, Sean Hooper, Iain Anderson, Amrita Pati, Natalia N. Ivanova, Athanasios Lykidis, Adam Zemla)

• Adopt a microbe education project (Cheryl Kerfeld)• Outreach (David Gilbert)• $$$ (DOE, Eddy Rubin, Jim Bristow)


Assess Benefits of GEBA

• All genomes have some value

• But what, if any, is the benefit of tree-guided sequencing over other selection methods

• Lessons for other large scale microbial genome projects?


GEBA Lesson 1

rRNA Tree is Useful for Identifying Phylogenetically Novel Genomes

rRNA Tree topology is not perfect;Genome-based trees better


rRNA Tree of Life

Based on tree by

Norm Pace


Wh

Whole genome tree built using AMPHORAby Martin Wu and Dongying Wu


PD of rRNA, Genome Trees Similar

From Wu et al. 2009. http://www.nature.com/nature/journal/v462/n7276/full/nature08656.html


http://www.nature.com/nature/journal/v462/n7276/full/nature08656.html


Proteobacteria


GEBA Lesson 2

Phylogenetically-guided genome selection improves genome

annotation


Predicting Function

• Key step in genome projects• More accurate predictions help guide

experimental and computational analyses• Many diverse approaches• Comparative and evolutionary analysis

greatly improves most predictions


Most/All Functional Prediction Improves w/ Better Phylogenetic Sampling

• Better definition of protein family sequence “patterns”

• Conversion of hypothetical into conserved hypotheticals

• Greatly improves “comparative” and “evolutionary” based predictions

• Linking distantly related members of protein families

• Improved non-homology prediction


GEBA Lesson 3

Improves analysis of genome data from uncultured organisms


Environmental Shotgun Sequencing

shotgun

clone


rRNA phylotyping from metagenomics

Venter et al., 2004


Shotgun Sequencing Allows Use of Alternative Anchors (e.g., RecA)

Venter et al., 2004


0

0.1250

0.2500

0.3750

0.5000

Alphaproteobacteria

Betaproteobacteria

Gammaproteobacteria

Epsilonproteobacteria

Deltaproteobacteria

Cyanobacteria

Firmicutes

Actinobacteria

Chlorobi

CFB

Chloroflexi

Spirochaetes

Fusobacteria

Deinococcus-Thermus

Euryarchaeota

Crenarchaeota

Sargasso Phylotypes

Wei

ght

ed %

of

Clo

nes

Major Phylogenetic Group

EFGEFTuHSP70RecARpoBrRNA

Shotgun Sequencing Allows Use of Other Markers

Venter et al., 2004


0

0.1250

0.2500

0.3750

0.5000

Alphaproteobacteria

Betaproteobacteria

Gammaproteobacteria

Epsilonproteobacteria

Deltaproteobacteria

Cyanobacteria

Firmicutes

Actinobacteria

Chlorobi

CFB

Chloroflexi

Spirochaetes

Fusobacteria

Deinococcus-Thermus

Euryarchaeota

Crenarchaeota

Sargasso Phylotypes

Wei

ght

ed %

of

Clo

nes

Major Phylogenetic Group

EFGEFTuHSP70RecARpoBrRNA

Shotgun Sequencing Allows Use of Other Markers

Venter et al., 2004

Cannot be done without good sampling of genomes


ABCDEFG

TUVWXYZ

Binning challenge


ABCDEFG

TUVWXYZ

Binning challenge

Best binning method: reference genomes


ABCDEFG

TUVWXYZ

Binning challenge

No reference genome? What do you do?


ABCDEFG

TUVWXYZ

Binning challenge

No reference genome? What do you do?

Phylogeny ....Saturday, April 24, 2010

Phylogenetic Binning Using AMPHORA

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Alph

apro

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acteria

Betapr

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ia

Gammap

roteob

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Deltapr

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bacter

ia

Epsil

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ssified

Pro

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Cyan

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Chlamyd

iae

Acidob

acteria

Bacter

oide

tes

Actin

obac

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Aquific

ae

Plan

ctom

ycetes

Spiro

chae

tes

Firmicu

tes

Chloro

flexi

Chloro

bi

Uncla

ssified

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dnaGfrrinfCnusApgkpyrGrplArplBrplCrplDrplErplFrplKrplLrplMrplNrplPrplSrplTrpmArpoBrpsBrpsCrpsErpsIrpsJrpsKrpsMrpsSsmpBtsf

AMPHORA - each read on its own treeSaturday, April 24, 2010

Phylogenetic Binning Using AMPHORA

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Alph

apro

teob

acteria

Betapr

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Gammap

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Deltapr

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Epsil

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Cyan

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dnaGfrrinfCnusApgkpyrGrplArplBrplCrplDrplErplFrplKrplLrplMrplNrplPrplSrplTrpmArpoBrpsBrpsCrpsErpsIrpsJrpsKrpsMrpsSsmpBtsf

AMPHORA - each read on its own tree

Cannot be done without good sampling of genomes


GEBA Phylogenomic Lesson 5

We have still only scratched the surface of microbial diversity


Protein Family Rarefaction Curves

• Take data set of multiple complete genomes• Identify all protein families using MCL• Plot # of genomes vs. # of protein families


Phylogenetic Distribution Novelty: Bacterial Actin Related Protein

Haliangium ochraceum DSM 14365 Patrik D’haeseleer, Adam Zemla, Victor Kunin

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From Wu et al. 2009. http://www.nature.com/nature/journal/v462/n7276/full/nature08656.htmlSaturday, April 24, 2010



rRNA Tree of Life

Based on tree by

Norm Pace


Phylogenetic Diversity: Sequenced Bacteria & Archaea





Phylogenetic Diversity with GEBA





Phylogenetic Diversity: Isolates

From Wu et al. 2009. http://www.nature.com/nature/journal/v462/n7276/full/nature08656.htmlSaturday, April 24, 2010



Phylogenetic Diversity: All





Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter



• Most phyla with cultured species are sparsely sampled

• Lineages with no cultured taxa even more poorly sampled

Well sampled phylaPoorly sampled

No cultured taxaSaturday, April 24, 2010

Uncultured Lineages:Technical Approaches

• Get into culture• Enrichment cultures• If abundant in low diversity ecosystems• Flow sorting• Microbeads• Microfluidic sorting• Single cell amplification


GEBA Phylogenomic Lesson 6

Need Experiments from Across the Tree of Life too


Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter


As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter


• Experimental studies are mostly from three phyla

As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter


• Experimental studies are mostly from three phyla

• Some studies in other phyla

As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter




• Same trend in Eukaryotes

As of 2002



Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter




• Same trend in Viruses

As of 2002



0.1

Acidobacteria

Bacteroides

Fibrobacteres

Gemmimonas

Verrucomicrobia

Planctomycetes

Chloroflexi

Proteobacteria

Chlorobi


Cyanobacteria

Chlamydia

Spriochaetes


Thermotogae

TM6OS-K

Termite GroupOP8

Marine GroupAWS3

OP9

NKB19

OP3

OP10

TM7

OP1OP11

Nitrospira



Chrysiogenetes

Thermomicrobia

Dictyoglomus

Coprothmermobacter

Tree based on Hugenholtz (2002) with some modifications.

Need experimental studies from across the tree too


MICROBES


A Happy Tree of Life


Lateral transfer

• Many lines of evidence suggest it is important in adaptations in microbes– E.g., K12 vs. O157:H7– e.g., Many genes show anomalous patterns

• However, does not appear to wipe out phylogenetic signal– Core of genomes gives similar phylogeny– Most acquired genes do not last long in lineages– Many claims of LGT are more “identification of

anomalies” than detecting LGT


a phylogeny driven genomic encyclopedia of bacteria and archaea

Education

thebacterial tree

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