A phylogeny driven genomic encyclopedia of bacteria and archaea

A phylogeny driven genomic
encyclopedia of bacteria and archaea

Jonathan A. Eisen

Talk at Stanford University
April 17, 2010
Saturday, April 24, 2010

Bacterial evolve


Fleischmann et al.
1995

Microbial genomes

From http://genomesonline.org

rRNA Tree of Life

Based on
tree by
Norm Pace


The Tree is not Happy

Based on
tree by
Norm Pace


As of 2002 Proteobacteria
TM6
OS-K • At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Bacteroides bacteria
Chlorobi
Fibrobacteres
Marine GroupA
WS3
Gemmimonas
Firmicutes
Fusobacteria
Actinobacteria
OP9
Cyanobacteria
Synergistes
Deferribacteres
Chrysiogenetes
NKB19
Verrucomicrobia
Chlamydia
OP3
Planctomycetes
Spriochaetes
Coprothmermobacter
OP10
Thermomicrobia
Chloroﬂexi
TM7
Deinococcus-Thermus
Dictyoglomus
Aquiﬁcae
Thermudesulfobacteria
Thermotogae
OP1 Based on
OP11 Hugenholtz, 2002

TM6
OS-K
• At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Chlorobi
Fibrobacteres
Marine GroupA • Genome
WS3
Gemmimonas
Firmicutes
sequences are
Fusobacteria
Actinobacteria
mostly from
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
Verrucomicrobia
Chlamydia
OP3
Planctomycetes
Spriochaetes
Coprothmermobacter
OP10
Thermomicrobia
Chloroﬂexi
TM7
Deinococcus-Thermus
Dictyoglomus
Aquiﬁcae
Thermotogae
OP1 Based on

TM6
OS-K
• At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Chlorobi
Fibrobacteres
WS3
Gemmimonas
Firmicutes
sequences are
Fusobacteria
Actinobacteria
mostly from
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
• Some other
Verrucomicrobia
Chlamydia
OP3
phyla are
Planctomycetes
Spriochaetes only sparsely
Coprothmermobacter
OP10
Thermomicrobia
sampled
Chloroﬂexi
TM7
Deinococcus-Thermus
Dictyoglomus
Aquiﬁcae
Thermotogae
OP1 Based on

TM6
OS-K
• At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Chlorobi
Fibrobacteres
WS3
Gemmimonas
Firmicutes
sequences are
Fusobacteria
Actinobacteria
mostly from
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
• Some other
Verrucomicrobia
Chlamydia
OP3
phyla are
Planctomycetes
Coprothmermobacter
OP10
Thermomicrobia
sampled
Chloroﬂexi
TM7
Deinococcus-Thermus
• Same trend in
Dictyoglomus
Aquiﬁcae
Archaea
Thermotogae
OP1 Based on

TM6
OS-K
• At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Chlorobi
Fibrobacteres
WS3
Gemmimonas
Firmicutes
sequences are
Fusobacteria
Actinobacteria
mostly from
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
• Some other
Verrucomicrobia
Chlamydia
OP3
phyla are
Planctomycetes
Coprothmermobacter
OP10
Thermomicrobia
sampled
Chloroﬂexi
TM7
Deinococcus-Thermus
• Same trend in
Dictyoglomus
Aquiﬁcae
Eukaryotes
Thermotogae
OP1 Based on

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


Proteobacteria
• NSF-funded TM6
OS-K
• At least 40
Tree of Life Acidobacteria
Termite Group phyla of
OP8
Project Nitrospira
Chlorobi
• A genome Fibrobacteres
WS3
from each of Gemmimonas sequences are
Firmicutes
eight phyla Fusobacteria
mostly from
Actinobacteria
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
• Some other
Verrucomicrobia
Chlamydia
OP3
phyla are only
Planctomycetes
Spriochaetes sparsely
Coprothmermobacter
OP10
Thermomicrobia
sampled
Chloroﬂexi
TM7
Deinococcus-Thermus
• Solution I:
Dictyoglomus
Aquiﬁcae sequence more
Eisen & Ward, PIs Thermudesulfobacteria
Thermotogae
OP1 phyla
OP11


Organisms Selected
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)


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


The Tree of Life is Still Angry


Major Lineages of Actinobacteria
2.5 Actinobacteria
2.5.1 Acidimicrobidae
2.5.1 Acidimicrobidae 2.5.1.1 Unclassified
2.5.1.2 "Microthrixineae
2.5.1.1 Unclassified 2.5.1.3 Acidimicrobineae
2.5.1.3.1 Unclassified
2.5.1.2 "Microthrixineae 2.5.1.3.2 Acidimicrobiaceae
2.5.1.4 BD2-10
2.5.1.3 Acidimicrobineae 2.5.1.5 EB1017
2.5.2 Actinobacteridae
2.5.1.4 BD2-10 2.5.2.1 Unclassified
2.5.2.10 Ellin306/WR160
2.5.1.5 EB1017 2.5.2.11 Ellin5012
2.5.2.12 Ellin5034
2.5.2 Actinobacteridae 2.5.2.13 Frankineae
2.5.2.1 Unclassified 2.5.2.13.2 Acidothermaceae

2.5.2.10 Ellin306/WR160 2.5.2.13.3
2.5.2.13.4
Ellin6090
Frankiaceae

2.5.2.11 Ellin5012 2.5.2.13.5
2.5.2.13.6
Geodermatophilaceae
Microsphaeraceae

2.5.2.12 Ellin5034 2.5.2.13.7
2.5.2.14
Sporichthyaceae
Glycomyces
2.5.2.13 Frankineae 2.5.2.15
2.5.2.15.1
Intrasporangiaceae
Unclassified
2.5.2.14 Glycomyces 2.5.2.15.2
2.5.2.15.3
Dermacoccus
Intrasporangiaceae
2.5.2.15 Intrasporangiaceae 2.5.2.16
2.5.2.17
Kineosporiaceae
Microbacteriaceae
2.5.2.16 Kineosporiaceae 2.5.2.17.1
2.5.2.17.2
Unclassified
Agrococcus
2.5.2.17 Microbacteriaceae 2.5.2.17.3
2.5.2.18
Agromyces
Micrococcaceae
2.5.2.18 Micrococcaceae 2.5.2.19
2.5.2.2
Micromonosporaceae
Actinomyces
2.5.2.19 Micromonosporaceae 2.5.2.20
2.5.2.20.1
Propionibacterineae
Unclassified
2.5.2.2 Actinomyces 2.5.2.20.2
2.5.2.20.3
Kribbella
Nocardioidaceae
2.5.2.20 Propionibacterineae 2.5.2.20.4
2.5.2.21
Propionibacteriaceae
Pseudonocardiaceae
2.5.2.21 Pseudonocardiaceae 2.5.2.22
2.5.2.22.1
Streptomycineae
Unclassified
2.5.2.22 Streptomycineae 2.5.2.22.2
2.5.2.22.3
Kitasatospora
Streptacidiphilus
2.5.2.23 Streptosporangineae 2.5.2.23
2.5.2.23.1
Streptosporangineae
Unclassified
2.5.2.3 Actinomycineae 2.5.2.23.2
2.5.2.23.3
Ellin5129
Nocardiopsaceae
2.5.2.4 Actinosynnemataceae 2.5.2.23.4
2.5.2.23.5
Streptosporangiaceae
Thermomonosporaceae
2.5.2.5 Bifidobacteriaceae 2.5.2.3 Actinomycineae
2.5.2.4 Actinosynnemataceae
2.5.2.6 Brevibacteriaceae 2.5.2.5 Bifidobacteriaceae
2.5.2.6 Brevibacteriaceae
2.5.2.7 Cellulomonadaceae 2.5.2.7 Cellulomonadaceae
2.5.2.8 Corynebacterineae
2.5.2.8 Corynebacterineae 2.5.2.8.1 Unclassified
2.5.2.8.2 Corynebacteriaceae
2.5.2.9 Dermabacteraceae 2.5.2.8.3 Dietziaceae
2.5.2.8.4 Gordoniaceae
2.5.3 Coriobacteridae 2.5.2.8.5 Mycobacteriaceae
2.5.2.8.6 Rhodococcus
2.5.3.1 Unclassified 2.5.2.8.7 Rhodococcus
2.5.2.8.8 Rhodococcus
2.5.3.2 Atopobiales 2.5.2.9 Dermabacteraceae
2.5.3.3 Coriobacteriales 2.5.2.9.2 Brachybacterium
2.5.2.9.3 Dermabacter
2.5.3.4 Eggerthellales 2.5.3 Coriobacteridae
2.5.3.1 Unclassified
2.5.4 OPB41 2.5.3.2 Atopobiales
2.5.3.3 Coriobacteriales
2.5.5 PK1 2.5.3.4 Eggerthellales
2.5.4 OPB41
2.5.6 Rubrobacteridae 2.5.5 PK1
2.5.6 Rubrobacteridae
2.5.6.1 Unclassified 2.5.6.1 Unclassified
2.5.6.2 "Thermoleiphilaceae
2.5.6.2 "Thermoleiphilaceae 2.5.6.2.1 Unclassified
2.5.6.2.2 Conexibacter
2.5.6.3 MC47 2.5.6.2.3 XGE514
2.5.6.3 MC47
2.5.6.4 Rubrobacteraceae 2.5.6.4 Rubrobacteraceae


Proteobacteria
TM6
OS-K
• At least 100 phyla of
Acidobacteria
Termite Group
OP8
bacteria
Nitrospira
Bacteroides
Chlorobi
• Genome sequences are
Fibrobacteres
Marine GroupA mostly from three phyla
WS3
Gemmimonas
Firmicutes • Most phyla with cultured
Fusobacteria
Actinobacteria species are sparsely
OP9
Cyanobacteria
Synergistes
sampled
Deferribacteres
Chrysiogenetes
NKB19 • Lineages with no cultured
Verrucomicrobia
Chlamydia
OP3
taxa even more poorly
Planctomycetes
Spriochaetes sampled
Coprothmermobacter
OP10
Thermomicrobia
Chloroflexi
• Solution - use tree to really
TM7
Deinococcus-Thermus fill gaps
Dictyoglomus
Aquificae Well sampled phyla
Thermotogae
OP1
OP11


http://www.jgi.doe.gov/programs/GEBA/pilot.html

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


B:
Ac
tin
ob
ac
te
B: ria # of Genomes
Am (H

in igh

10
15
20
25
30
35

0
5
an G
a C
B: B: er )
Ba Aq ob
ct uif ia
B: ero ica
B: e
D Ch ide
B: e ef lo te
r s
D rri ofl
ef ba e
B: e c xi
B: De B rrib ter
Ep lta : D act es
si Pr ei er
lo o n es
n te oc
Pr ob oc
ot a ci
B: e ct
G B: oba eri
am B F ct a
: ir e
B: m Fu mi ria
a
G P so cut
em ro ba e
t c s
B: ma eo te
ba ri
H tim c a
a t
B: loa ona eri
a
B: Pl nae de
an r te
Th c o s

Phyla
er B: to bia
m S m le
y s
B: od piro ce
es c te
T u h
B: he lfo ae s
rm b te
GEBA Pilot Target List

Th o a s
er de cte
m s ri
u a
A: ove lfo
H n bi
A: alo abu a
A: A b la
M rc ac e
A: et ha te
M han eo ria
et g
ha ob lob
ac i
A: no te
m r
A: The icr ia
Th rm obi
er oc a
m oc
op ci
ro
te
i

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

Wh

Whole genome tree
built using
AMPHORA
by 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

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

Weighted % of Clones

0
0.1250
0.2500
0.3750
0.5000
Al
ph
ap
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t eo
Be b ac
ta
pr t er
ot
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am

ac
m t er
ap ia
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np t er
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De t eo
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b
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ac
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Fi ia
rm
ic
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Ac s
tin
ob
ac
ter
C ia
hl
or
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i
C
FB

Major Phylogenetic Group
Sargasso Phylotypes

C
hl
or
of
le
Sp xi
iro
ch
ae
te
Fu
so s
De ba
in ct
er
oc ia
oc
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ry r
ar mu
ch s
ae
C ot
re a
na
rc
ha
eo
ta
Shotgun Sequencing Allows Use of Other Markers

Venter et al., 2004
EFG
EFTu

rRNA
RecA
RpoB
HSP70

Weighted % of Clones

0
0.1250
0.2500
0.3750
0.5000
Al
ph
ap
ro
t eo
Be b ac
ta
pr t er
ot
e ia
G ob
am

ac
m t er
ap ia
ro
Ep te
si ob
lo ac
np t er
ro ia
De t eo
lta ba
ct
pr
ot e ria
eo
b
C ac
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n ob ia
ac
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Fi ia
rm
ic
u te
Ac s
tin
ob
ac
ter
C ia
hl
or
ob
i
without good

C
FB

Major Phylogenetic Group
Sargasso Phylotypes

C
Cannot be done

hl
or
of
le
Sp xi
iro
ch
ae
te
Fu
so s
De ba
in ct
er
oc ia
sampling of genomes

oc
cu
s-
Eu The
ry r
ar mu
ch s
ae
C ot
re a
na
rc
ha
eo
ta
Shotgun Sequencing Allows Use of Other Markers

Venter et al., 2004
EFG
EFTu

rRNA
RecA
RpoB
HSP70

Binning challenge

A T
B U
C V
D W
E X
F Y
G Z

Binning challenge

A T
B U
C V
D W
E X
F Y
G Best binning method: reference genomes Z

Binning challenge

A T
B U
C V
D W
E X
F Y
G No reference genome? What do you do? Z

Binning challenge

A T
B U
C V
D W
E X
F Y
G No reference genome? What do you do? Z
Phylogeny ....

Al
ph
ap
ro
Be te
ta o ba
G p

0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
am ro ct
te er
m o ia
ap ba

ro ct
D te er
el ob ia
ta
pr ac
Ep ot te
U si
lo eo ria
nc ba
la np
ct
ss ro er
ifi te ia
ed ob
Pr ac
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Cy ct
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ob ia
ac
Ch te
ria
la
m
Ac yd
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ct ria
er
Ac oi
de
tin te
ob s
ac
te
ria
Aq
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an fic
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om ae
yc
Sp et

AMPHORA - each read on its own tree
iro es
ch
ae
Fi te
rm s
ic
ut
Ch es
lo
ro
U fle
nc xi
la Ch
ss lo
ifi ro
ed bi
Ba
ct
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ia
Phylogenetic Binning Using AMPHORA
frr

tsf
pgk

rplL
rplF

rplP

rplT
rplE
infC

rpsI
rplS
rplA
rplB

rplK
rplC

rpsJ
rplN
rplD

rplM

rpsE

rpsS
rpsB

rpsK
rpsC
rpoB

rpsM
pyrG
nusA
dnaG

rpmA

smpB

Phylogenetic Binning Using AMPHORA
dnaG
0.7
frr
infC
0.6 nusA
pgk
pyrG
0.5

0.4
Cannot be done rplA
rplB
rplC
rplD

0.3 without good rplE
rplF
rplK
rplL
0.2

0.1
sampling of genomes rplM
rplN
rplP
rplS
rplT
rpmA
0 rpoB
rpsB

es
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AMPHORA - each read on its own tree

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
2"#3)&4&*&& !"#*)$*),+%
5"#$-.-6&0&1- !"#$%,$-%)(
7"#0(1.8-9& !"#$''+-+,',!
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*$ $++ ;"#01,&-*0 !"#*+,$*'(
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$++ B"#A1%%/0# "#%*,-&*'(
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$++ ;"#01,&-*0 !"#*+,$*),!
;"#)$C.1$-/@ !"#&&),(*((- +!&'
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(( !"#(C1%&1*1 !"#$-,(%'+-!
(% 5"#$-.-6&0&1- !"#$,+$(,&
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-) ?"#4&0$)&4-/@ !"#''-+&%$-
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$++ <"#@/0$/%/0 !"#&&'&%'*(, !&'(0

+/*!

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

Phylogenetic Diversity:
Sequenced Bacteria & Archaea


Phylogenetic Diversity with GEBA


Phylogenetic Diversity: Isolates


Phylogenetic Diversity: All


Proteobacteria
TM6
OS-K
• At least 40 phyla of
Acidobacteria
Termite Group
OP8
bacteria
Nitrospira
Bacteroides
Chlorobi
• Genome sequences are
Fibrobacteres
Marine GroupA mostly from three phyla
WS3
Gemmimonas
Firmicutes • Most phyla with cultured
Fusobacteria
Actinobacteria species are sparsely
OP9
Cyanobacteria
Synergistes
sampled
Deferribacteres
Chrysiogenetes
NKB19 • Lineages with no cultured
Verrucomicrobia
Chlamydia
OP3
taxa even more poorly
Planctomycetes
Spriochaetes sampled
Coprothmermobacter
OP10
Thermomicrobia
Chloroﬂexi
TM7
Deinococcus-Thermus
Dictyoglomus
Aquiﬁcae Well sampled phyla
Thermotogae Poorly sampled
OP1
OP11
No cultured taxa

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


TM6
OS-K
• At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Chlorobi
Fibrobacteres
Marine GroupA • Experimental
WS3
Gemmimonas
Firmicutes
studies are
Fusobacteria
Actinobacteria
mostly from
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
Verrucomicrobia
Chlamydia
OP3
Planctomycetes
Spriochaetes
Coprothmermobacter
OP10
Thermomicrobia
Chloroﬂexi
TM7
Deinococcus-Thermus
Dictyoglomus
Aquiﬁcae
Thermotogae
OP1 Based on

TM6
OS-K
• At least 40
Acidobacteria
Termite Group
OP8
phyla of
Nitrospira
Chlorobi
Fibrobacteres
Marine GroupA • Experimental
WS3
Gemmimonas
Firmicutes
studies are
Fusobacteria
Actinobacteria
mostly from
OP9
Cyanobacteria
Synergistes
three phyla
Deferribacteres
Chrysiogenetes
NKB19
• Some studies
Verrucomicrobia
Chlamydia
OP3
in other phyla
Planctomycetes
Spriochaetes
Coprothmermobacter
OP10
Thermomicrobia
Chloroﬂexi
TM7
Deinococcus-Thermus
Dictyoglomus
Aquiﬁcae
Thermotogae
OP1 Based on

A phylogeny driven genomic encyclopedia of bacteria and archaea

A phylogeny driven genomic encyclopedia of bacteria and archaea

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