Ancestral Sequence Reconstruction

267 Pages·2007·5.73 MB·English

by  David A. Liberles

Ancestral Sequence Reconstruction
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Ancestral Sequence
Reconstruction
EDITED BY
David A. Liberles
University of Wyoming, Laramie, WY, USA
1
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Contents
Foreword andintroduction vii
Introduction tothemeetinginKristineberg, Sweden x
Contributors xii
I Introductory scientificoverview
1 The earlydaysofpaleogenomics: connectingmolecules totheplanet 3
StevenA.Benner
2 Ancestral sequence reconstructionasatooltounderstandnatural
history andguidesynthetic biology:realizingandextendingthevision
of ZuckerkandlandPauling 20
EricA.Gaucher
3 Linkingsequence tofunctionindrugdesign withancestral
sequence reconstruction 34
JanosT.Kodra,MarieSkovgaard,DennisMadsen,andDavidA.Liberles
II Computational methodology andconcerns
4 Probabilistic modelsandtheirimpactontheaccuracy ofreconstructed
ancestral proteinsequences 43
TalPupko,AdiDoron-Faigenboim, DavidA.Liberles,and GinaM.Cannarozzi
5 Probabilistic ancestralsequencesbasedontheMarkovianmodelof
evolution: algorithmsandapplications 58
GinaM.Cannarozzi,Adrian Schneider,and GastonH.Gonnet
6 Estimating thehistoryofmutationsonaphylogeny 69
JonathanP.Bollback,PaulP.Gardner,andRasmusNielsen
7 Coarse projectionsoftheprotein-mutationalfitnesslandscape 80
F.Nicholas Braun
8 Dealingwithuncertaintyinancestralsequence reconstruction: sampling
fromtheposterior distribution 85
DavidD.Pollockand BelindaS.W.Chang
9 Evolutionary propertiesofsequencesandancestralstatereconstruction 95
LesleyJ.CollinsandPeterJ.Lockhart
v
vi CONTENTS
10Reconstructing theancestraleukaryote:lessonsfromthepast 103
MaryJ.O’ConnellandJamesO. McInerney
III Computational applicationsofancestralsequence reconstruction
11Usingancestralsequence inferencetodeterminethetrendoffunctional
divergence aftergene duplication 117
XunGu,YingZheng,Yong Huang,andDongpingXu
12Reconstruction ofancestralproteomes 128
ToniGabaldo´nandMartijnA.Huynen
13Computational reconstruction ofancestralgenomicregions from
evolutionarily conserved geneclusters 139
EtienneG.J.Danchin,EricA.Gaucher,and PierrePontarotti
IV Experimentalmethodology andconcerns
14Experimental resurrectionofancientbiomolecules: genesynthesis,
heterologous proteinexpression,andfunctionalassays 153
EricA.Gaucher
15Dealingwithmodeluncertaintyinreconstructing ancestralproteinsin
thelaboratory: examplesfromarchosaurvisualpigmentsandcoral
fluorescent proteins 164
BelindaS.W.Chang, MikhailV.Matz,StevenF.Field,Johannes Mu¨ller,
andIlkevan Hazel
V Experimentalsynthesisofancestralproteinstotest
biological hypotheses
16Usingancestralgene resurrectiontounraveltheevolutionof
protein function 183
JosephW.ThorntonandJamieT.Bridgham
17A thermophiliclastuniversalancestorinferred fromitsestimated
aminoacidcomposition 200
DawnJ.Brooks andEricA.Gaucher
18The resurrectionofribonucleases frommammals:fromecologytomedicine 208
SlimO.SassiandStevenA.Benner
19Evolution ofspecificity anddiversity 225
DenisC.Shields,Catriona R.Johnston,IainM.Wallace,andRichard J.Edwards
Conclusions andawayforward 236
DavidA.Liberles
Index 239
Foreword and introduction
With the realization that the combination of com- within a gene represented the homologous site,
putational reconstruction of ancestral protein wheresubstitutionmodelsshouldthenbeapplied
sequences andthe experimental synthesis ofthese tocharacterizeitsevolution.Thisisthetraditional
proteins could be used to test specific molecular, view of homology as embodied in the vast litera-
biomedical, ecological, and evolutionary hypoth- tures of molecular evolution and population
eses, this methodological combination has been genetics.However,RichardGoldstein(whohasin
used with increasing popularity. Because a num- the past generated substitution matrices that
ber of scientific issues surround the use of ances- characterize substitution differentially between
tral sequence reconstruction that need to be different structural elements) and David Pollock
fleshed out, a scientific meeting was organized to took a structural perspective on homology,
discuss the use of ancestral sequence reconstruc- arguing that a homologous position might some-
tion. Beyond procedures and pitfalls, a number of timesbebetterdefinedbythestructuralattributes
new applications of ancestral sequence recon- constraining it in a three-dimensional structure
structionhavebeguntoemergeandapresentation rather than the position within a gene sequence.
of several of these was deemed valuable. For example, position 3 in an a-helix could be
With funding from the European Science aligned with position 3 in the homologous a-helix
Foundation (ESF), Vetenskapsra˚det (the Swedish ofanotherprotein,eveniftheyrepresentpositions
Research Council), and the Linnaeus Centre for 65and68inthegenesequenceandnoinsertionor
Bioinformatics (Uppsala University, Sweden), deletion events have occurred. This latter view
David Ardell (Uppsala University, Sweden), requires the use of different types of substitution
Giorgio Matassi (University of Paris VI, France), modelsthantheformerview,sothedivergenceof
and I organized a meeting entitled, ‘‘Using opinion has practical as well as philosophical
Ancestral Sequence Reconstruction to Understand concerns.
Protein Function’’ in Kristineberg, Sweden, on Another active area of discussion involved sour-
30–31 March 2005. The meeting consisted of 38 cesofbiasandanongoingdiscussionofthevalidity
participants from 12 different countries attending of using maximum-likelihood or -parsimony
18 scientific presentations. Following the meeting ancestralsequencereconstructionscomparedwitha
and the vibrant discussion, it was decided that a sampling fromthe posterior distribution ofa Baye-
book involving chapters by those attending the sian ancestral sequence reconstruction. The discus-
meeting and others in the field would be worth- sionatthemeeting(inadditiontoChapter8inthis
while, which was the origin of this project. volume) has spawned an active discussion in the
One philosophical discussion that emerged was peer-reviewed scientific literature. The argument is
on the true meaning of homology and what a that the maximum-likelihood or maximum-parsi-
homologoussiteiswhenasequenceslidesthrough mony ancestral sequence is under-represented by
a structure generating diverging alignments from rare variants, such as hydrophobic residues on the
sequence and structure-based methods. surface, that ultimately attribute overly stable or
David Ardell (in his lecture in Sweden) presented overly active properties to the reconstructed ances-
examples of cases where the two diverged and tor. It is argued that this is avoided by sampling
recommended sequence analysis using a DNA- from the posterior distribution, even if sampling
based view of homology, where a single position from the posterior results in less accurate
vii
viii FOREWORD AND INTRODUCTION
reconstruction at the sequence level. The experi- strategies and applications of using ancestral
mental implications of this proposal are presented sequence data to reconstruct entire proteomes. In
in both Chapters 8 and 15. A brief rebuttal to this work not presented in this book, David Haussler
view and defense of maximum likelihood is pre- and colleagues have extended this type of
sented by Eric Gaucher in Chapter 2. Further ana- approach to reconstructing the entire genome of
lysisanddiscussionsofthistopicaresuretoappear the last common ancestor of mammals. The
in the literature overthe coming years. thoughtful introduction by Emile Zuckerkandl
A third topic raised for discussion at the proposes further extension of the analysis from
meetingbyGiorgioMatassiwas,‘‘Areallproteins entire proteomes to interactomes and the field,
reconstructable?’’ Clearly some proteins, like the although not there yet, will surely move in this
green fluorescent protein-like proteins worked on direction.
byMikhailMatzandcolleagues(andpresentedin Moving to experimental work to test computa-
Chapter 15) are more amenable to experimental tional hypotheses, Chapters 14 and 15 present
study than other proteins. However, functional strategies for converting computationally recon-
assays in vitro or in vivo are indeed available for structed ancestral sequences to proteins resur-
a great many proteins. Chapter 17 presents a rected in the laboratory. Chapter 15 includes an
reconstruction back to the last universal ancestor expanded discussion of how to accommodate the
and other chapters deal with various complexities controversial computational strategy suggested in
in sequence evolution that will enable more accu- Chapter 8. Chapters 16–19 then address various
rate reconstruction. biological questions using ancestral sequence
The first two chapters provide a historical and reconstruction and resurrection, across different
scientific overview of ancestral sequence recon- evolutionary depths and drawing on widely dif-
struction, and Chapter 3 extends the use of the ferent scientific disciplines.
technique to applications of drug design and Rather than presenting a view that is consistent
mentions the companion technique of substitu- fromchaptertochapter,severalcontradictoryviews
tional mapping. A discussion of standard approa- arepresenteddifferentlybydifferentauthorstogive
ches for ancestral sequence reconstruction is readers a chance to appreciate ongoing debates in
presented in Chapters 4 and 5, with Chapter 6 the field and formulate their own opinions. In the
presenting a method (with a companion software concludingsection,Iprovidealistofseveralavail-
package) for substitutional mapping. ablesoftwarepackagesthatareavailabletoperform
Chapters7and8presentsomeofthelimitations different analyses described in the book. I also
and considerations that should go into computa- attempt to tie together some of the discussion to
tionally reconstructing ancestors, including meth- presenttheexperimentalmolecularbiologistwitha
odological sources of bias and biophysical potentialwayforwardinattemptingthesemethods
implications. Chapter 9 presents a discussion of intheirownlaboratory.
covarion or heterotacheous processes, where Theimageofcrocodiliansonthebookcoverwas
sites shift rates due to intra- or intermolecular generated with the enthusiastic help of John
coevolution, and their effects on ancestral Brueggen at the St. Augustine Alligator Farm
sequence reconstruction. Chapter 10 analyzes Zoological Park (http://www.alligatorfarm.us).
some controversies in our knowledge of the The picture shows all 23 extant species of croco-
referencespeciestreeandhowdifferenttopologies dilans and as a Postdoctoral Researcher at Uni-
can affect reconstructed ancestral sequences. The versity of Florida, I always enjoyed visiting the
covarion processes discussed in Chapter 9, while alligator farm and comparing the species in my
sometimes neutral, are also sometimes linked mind. While I have never worked with crocodi-
to functional shifts. Chapter 11 discusses metho- lians, one of the constant battles that my lab has
dology for linking this process to functional shifts faced is the search for DNA from different closley
after gene duplication using ancestral sequences. related species. Ultimately in this process, we are
Chapters 12 and 13 present computational interestedinaddressingthequestion,‘‘Whatwere
FOREWORD AND INTRODUCTION ix
the molecular events that made each species (especially Alexander Churbanov and Steven
unique from its closest relatives?’’ So, as you look Massey),andmywifeJessica,aswellastoauthors
at the crocodilians on the cover of the book, ask whotookthetimetoreviewotherchaptersinthis
yourself how these species are different, what the effort (a special thanks for extra effort go to Eric
molecular underpinnings of this are, what the Gaucher, Tal Pupko, and Denis Shields). I also
selective forces that drove this were, and how the needtothankIan ShermanandStefanie Gehrigat
techniques described in this book can help us Oxford University Press for their patience. Thank
answer these questions. youforyourinterestinthegrowingresearchfield.
I am grateful to the external reviewers of David A. Liberles
chapters for this book, notably Aoife McLysaght University of Wyoming,
(Trinity College, Ireland), Arthur Lesk (Pennsyl- Laramie, WY, USA
vania State University, USA), my research group