the more the merrier: the genomics of single, double and polysymbioses
DESCRIPTION
Talk by Jonathan Eisen at PAG2007TRANSCRIPT
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The more the merrier:the genomics of single, double and
polysymbiosesJonathan A. Eisen
U. C. Davis Genome Center
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The more the merrier:the metagenomics of single, double
and polysymbiosesJonathan A. Eisen
U. C. Davis Genome Center
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Outline
• Introduction– Symbionts– Phylogenomics
• Two endosymbiont genomics tales– Wolbachia– Sharpshooter
• Where next?
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Sources for the Origin of Novelty
• New biochemical functions– Evolution of new genes– Old genes with new functions– Mixing and matching existing genes
• Changes in uses of existing genes– Targeting– Regulation
• Acquisition of new functions– Recombination– Lateral gene transfer– Symbioses
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Endosymbioses Drove Eukaryotic Evolution
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“Nothing in biology makes senseexcept in the light of evolution.”
T. H. Dobzhansky (1973)
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Phylogenomic Analysis
• Evolutionary reconstructions greatly improve genome analyses
• Genome analysis greatly improves evolutionary reconstructions
• There is a feedback loop such that these should be integrated
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Wolbachia pipientis wMel
• Wolbachia are obligate, maternally transmitted intracellular symbionts
• Wolbachia infect many invertebrate species– Many cause male specific deleterious effects– Model system for studying sex ratio changes in hosts– Some are mutualistic (e.g., in filarial nematodes)
• wMel selected as model system because it infects Drosophila melanogaster
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Wolbachia Metagenomic Sequencing
shotgunshotgun
sequencesequence
Analysis led by Matin Wu in collaboration with lab of Scott O’Neill
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Genome Completed
Wu et al., PLoS Biology 2004
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alanine/glycine
Na+
alanine/glycine
Na+
alanine/glycine
Na+
proline/betaine
H+
proline/betaine
H+WD0168
WD0414
WD1046
WD1047
WD0330
Na+
glutamate/aspartate
Na+
WD0211
WD0229
glutamate/aspartate
ornithine
putrescineWD0957
H+ Na+H+ Na+
WD0316 WD0407
H+
WD1107WD1299WD1300WD1391WD0816WD0765
Mg2+
WD0375
H+ Zn2+/Cd2+
WD1042
ATPADP
Zn2+
WD0362WD0938WD0937
ATPADP
Fe3+
WD1136WD0153WD0897
glycerol-3-phosphate/hexose-6-phosphate
phosphateWD0619
H+
drugs
H+
drugs
WD0056
WD0248
H+
drugs
H+
drugs
WD1320
WD0384
H+
?
H+
?
WD0621
WD0099
H+
metabolite?
WD0470
H+
metabolite?
WD1033
H+WD0249
metabolite?
ATPADP
heme
WD0411WD1093WD0340
K+
WD1249
Na+H+
drugsATP
ADP WD0400
phosphate
ATPADP
ORF00100ORF00714ORF00927ORF00940
(2?)
H+
F-type ATPase
ATP ADP
WD1233WD0203WD0204WD0427WD0428WD0429WD0655WD0656
phosphoenolpyruvate
1,3-bisphosphoglycerate
3-phosphoglycerate
2-phosphoglycerate
pyruvate
acetyl-CoA
citrate
isocitrate
oxaloacetate
suc-CoAsuccinate
fumarate
malate
oxaloacetate
TCA CYCLE
glyceraldehyde-3P
fructose-1,6-P2
dihydroxyacetone-P
WD1238
WD0091
WD0451
WD1167
WD0868
WD0494
WD0690
WD0105
WD0791
WD1309WD0544WD0751
WD1209WD1210
WD0437WD0727WD1221WD1222
WD0492
WD1121
mannose-1P mannose-6PWD0695
MALATE WD0488 WD1177WD0416WD0473WD0751WD0325
Non-oxidative Pentose Phosphate Pathway
xylulose-5P
glyceraldehyde-3P
sedoheptulose-7P
fructose-6P
ribose-5P
ribulose-5P
glyceraldehyde-3P
WD0551WD0387
WD0387
WD0712
erythrose-4P
WD1151
glycerol-3P
WD0731
Amino Acid catabolism
GLUTAMATE glutamineWD1322
GLUTAMINE glutamateWD0535
CYSTEINE alanineWD0997
THREONINE glycineWD0617,WD0617
PROLINE glutamateWD0103
SERINE glycineWD1035
Fatty Acid Biosynthesis WD0985, WD0650, WD1083, WD1170, WD0085
PRPP
WD0036
Thiamine metabolismWD1109,WD0763,WD0029,WD0913,WD1018,WD1024
AMP,ADP,dAMP, dADP,ATP,dATP,ITP,dITP,IMP,XMP,GMP,GDP,dGDP,dGTP,dGMP
WD1142WD1305WD1023WD0786WD0867WD0337WD0786
WD0661WD1183WD0197WD0089WD0195WD0439WD0197
adenylosuccinate WD0786
Purine Metabolism
UMPUDP
WD0684WD1295WD0895WD0230WD1239WD0228WD0461
aspartate semialdehydeaspartateWD1029 WD0960 WD0954
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Mitochondrial Origin Unresolved
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Wolbachia Evolutionary Rate is Accelerated
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Endosymbiont Trends
• Compared to free-living relatives– Smaller genomes– Lower GC content– Higher pIs– Higher rates of sequence evolution
• Wolbachia shows ALL of these
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Explanations for Endosymbiont Differences with Free-Living Relatives
• Repair hypothesis– Loss of DNA repair genes leads to increased mutation rate
– Trends are the direct and indirect result of this increased mutation rate
• Population genetics hypothesis– Smaller effective population size leads to more genetic drift
– Trends are mostly the result of accumulation of slightly deleterious mutations
• PopGen explanations favored– Wolbachia has full suite of repair genes
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Endosymbiont Trends
• Compared to free-living relatives– Smaller genomes– Lower GC content– Higher pIs– Higher rates of sequence evolution
• Wolbachia shows ALL of these
• However ….
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Wolbachia Overrun by Mobile ElementsRepeatClass
Size(Median)
Copies Protein motifs/families IS Family Possible Terminal Inverted Repeat Sequence
1 1512 3 Transposase IS4 5’ ATACGCGTCAAGTTAAG 3’2 360 12 - New 5’ GGCTTTGTTGCAT CGCTA 3’3 858 9 Transposase IS492/IS110 5’ GGCTTTGTTGCAT 3’4 1404.5 4 Conserved hypothetical,
phage terminaseNew 5’ ATACCGCGAWTSAWTCGCGGTAT 3’
5 1212 15 Transposase IS3 5’ TGACCTTACCCAGAAAAAGTGGAGAGAAAG 3’6 948 13 Transposase IS5 5’ AGAGGTTGTCCGGAAACAAGTAAA 3’7 2405.5 8 RT/maturase -8 468 45 - -9 817 3 conserved hypothetical,
transposaseISBt12
10 238 2 ExoD -11 225 2 RT/maturase -12 1263 4 Transposase ???13 572.5 2 Transposase ??? None detected14 433 2 Ankyrin -15 201 2 - -16 1400 6 RT/maturase -17 721 2 transposase IS63018 1191.5 2 EF-Tu -19 230 2 hypothetical -
Wu et al. 2004
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Glassy Winged Sharpshooter
• Feeds on xylem sap• Can transmit Pierce’s
Disease agent from infected plants to uninfected plants like mosquitoes with malaria
• Potential bioterror agent• Needs to get amino-
acids and other nutrients from symbionts like aphids
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Xylem and Phloem
From Lodish et al. 2000
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Endosymbionts Present
Moran et al. Env. Microbiol. 5: 2003
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Long Term Mutualism
Moran et al. Env. Microbiol. 5: 2003
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Sharpshooter Shotgun Sequencing
shotgunshotgun
sequencesequence
400,000
100,000
200,000
300,000
500,000
600,000
1
Wu et al. PLoS Biology 2006
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400,000
100,000
200,000
300,000
500,000
600,000
1
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Genome Helps Resolve Phylogeny
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Higher Evolutionary Rates in Clade
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Endosymbiont Trends
• Compared to free-living relatives– Smaller genomes– Lower GC content– Higher pIs– Higher rates of sequence evolution
• Baumannia shows ALL of these
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Explanations for Endosymbiont Differences with Free-Living Relatives
• Repair hypothesis
• Population genetics hypothesis
• PopGen explanations favored
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Variation in Evolution RatesCorrelated with Repair Gene Presence
MutS MutL
+ +
+ +
+ +
+ +
_ _
_ _
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Explanations for Endosymbiont Differences with Each Other
• Repair hypothesis
• Population genetics hypothesis
• Repair explanations favored
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Polymorphisms in Metapopulation
• Data from ~200 hosts– 104 SNPs– 2 indels
• PCR surveys show that this is between host variation
• Much lower ratio of transitions:transversions than in Blochmannia
• Consistent with absence of MMR from Blochmannia
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Baumannia Predicted Metabolism
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No Amino-Acid Synthesis
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???????
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Suggested Methods for Binning Did Not Work Well
• Assembly– Only Baumannia generated good contigs
• Depth of coverage– Everything else 0-1X coverage
• Nucleotide composition– No detectible peaks in any vector we looked at
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Binning by Phylogeny?
• Identified putative genes
• Built phylogenetic trees
• Examined and classified trees
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Host Sequence?
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Wolbachia Sequence?
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CFB Phyla
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Sulcia symbionts in Sharpshooters
Moran et al. 2005
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Sulcia symbionts in Sharpshooters
Moran et al. 2005
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Binning by Phylogeny
• Four main “phylotypes”– Gamma proteobacteria (Baumannia)– Arthropoda (sharpshooter)– Bacteroidetes (Sulcia)– Alpha-proteobacteria (Wolbachia)
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Binning by Phylogeny
• Four main “phylotypes”– Gamma proteobacteria (Baumannia)– Arthropoda (sharpshooter)– Bacteroidetes (Sulcia) - only a.a. genes here– Alpha-proteobacteria (Wolbachia)
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Finished 130 kb of Sulcia
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Co-Symbiosis?
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What is Next?
• More endosymbioses– Diversity of host species– Diversity of symbionts– Diversity of biology
• Epibionts and other obligate symbioses• Commensals
– Human gut– Hotspring mats
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TIGRTIGR
Other peopleOther people
Mom and DadMom and Dad
H. OchmanH. OchmanF. RobbF. Robb
J. BattistaJ. Battista
E. OriasE. Orias
D. BryantD. BryantS. O’NeillS. O’Neill
M. EisenM. Eisen
N. MoranN. Moran
R. MyersR. Myers
C. M. CavanaughC. M. Cavanaugh
P. HanawaltP. Hanawalt
J. HeidelbergJ. HeidelbergN. WardN. Ward
J. VenterJ. Venter
C. FraserC. Fraser
S. SalzbergS. Salzberg
I. PaulsenI. Paulsen
$$$$$$
NSFNSFDOEDOE
NIHNIH
M. WuM. Wu
D. WuD. Wu
S. ChatterjiS. Chatterji
H. HuseH. Huse
A. HartmanA. Hartman
MooreMoore
VIVI
D. RuschD. Rusch
A. HalpernA. Halpern
Eisen Eisen GroupGroup
J. MorganJ. Morgan
JGIJGI
E. EisenstadtE. Eisenstadt
M. FrazierM. Frazier
T. WoykeT. Woyke
E. RubinE. Rubin
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Calyptogena magnifica symbionts
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C. magnifica symbiont sequencing
• Collaboration between Cavanaugh Lab at Harvard (Irene Newton led analysis), Eisen lab, and JGI (Woyke and others).
• Funded by DOE through CSP program and sequencing and closure done at JGI
• Annotation and analysis involved DOE (JGI, ORNL), Harvard, TIGR, Davis, et al.
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Ruthia magnifica
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Sulcia Role Categories
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A Streamlined Chemoautotrophic Machine
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Correlation of Endosymbiont Features
• Correlation makes it difficult to tease apart cause and effect
• Need examples where properties are decoupled
• May be the case in Baumannia with genome size
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Long Term Effects of Repair Loss
• Endosymbionts are model systems for understanding the consequences of loss of repair activities
• RecA lost in Buchnera and Blochmannia but kept in Baumannia and Wigglesworthia
• MutSL loss mentioned previously
• RecBCD present even in species without RecA
• Mfd present in many species without UvrABCD
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Endosymbionts and Extremophiles
Origin of New Functions
Species Evolution
Genome Dynamics
Phylogeny, Processes,
Biogeography,Convergence
Mutation, Selection,
Repair, Replication
Multiple Origins,Simple Communities
New genes,Changes in old genes,
AcquisitionEisenLab
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Comparative vs. Evolutionary Approaches
• Comparative approaches involve documenting similarities and differences
• Evolutionary approaches involve documenting how and why the similarities and differences arose
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Comparative vs. Evolutionary
Topic Comparative Evolutionary
Structure prediction for rRNA
Conserved regions Correlated changes along tree
Gene presence vs. phenotpye
Presence and absence of genes
Gain and loss, lateral transfer
Selection Degree and pattern of conservation
HKA, Ds/Dn
Functional prediction
Ranking by level of similarity
Predicting function from trees
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Phylogenomic Analysis
• Evolutionary reconstructions greatly improve genome analyses
• Genome analysis greatly improves evolutionary reconstructions
• There is a feedback loop such that these should be integrated