Table Of ContentMobileGeneticElements1:4,256–261;November/December2011;G2011LandesBioscience
HGT turbulence
Confounding phylogenetic influence of duplicative
horizontal transfer and differential gene conversion
Weilong Hao1,2,* and Jeffrey D. Palmer1
1DepartmentofBiology;IndianaUniversity;Bloomington,INUSA;2DepartmentofBiologicalSciences;WayneStateUniversity;Detroit,MIUSA
Keywords: horizontal gene transfer, gene conversion, maximum likelihood, mitochondria, chimeric gene, phylogeny reconstruction,
recombination, simulations
Horizontalgenetransfer(HGT)oftenleadstophylogeneticincongruence.When“duplicativeHGT”introducesasecond
copy of a pre-existing gene, the two copies may then engage in gene conversion, leading to phylogenetically mosiac
genes.WhenduplicativeHGTisfollowedbydifferentialgeneconversionamongdescendantlineages,asundertheDH-
DCmodel,phylogeneticanalysisisfurthercomplicated.ToexploretheeffectsofDH-DConphylogenyreconstruction,we
analyzed two sets of sequences: (1) an augmented set of plant mitochondrial atp1 sequences for which we recently
© p2ublishe0d evid1ence o2f DH-D C; aLnd (2a) a setnof simdulatedesequesnces forBwhichiweovariedsthe ecxtentiofechimernism, thce e.
numberofchimericgenesandnucleotidesubstitutionrates.Weshowthatthephylogeneticbehaviorofevolutionarily
chimericgenesishighlyvolatileanddependsonboththedegreeofchimerismandthenumberofdifferentiallychimeric
genespresentintheanalysis.Furthermore,weshowthatthepresenceofchimericgenesingenetreescanspuriously
affect the phylogenetic position of purely native sequences, especially by attracting these sequences toward basal
positionsintrees.Weproposetheterm“HGTturbulence”todescribethesecomplexeffects ofevolutionarilychimeric
genesonphylogenetic results.
Do not distribute.
Introduction between co-existing native and foreign divergence of the two parental sequences
copies.12 Furthermore, gene conversion from each other.17
Horizontal gene transfer (HGT) is very can occur in either a continuous or When properly recognized and dealt
common and of great importance in discontinuous manner.13,14 Overall, then, with, recombination poses few problems
bacterial evolution1,2 and is also relatively gene conversion can lead to a potentially for phylogenetic analysis and interpreta-
common in certain eukaryotic lineages.3,4 complex and diverse set of patchwork tion. In practice, however, recombination
One consequence of HGT is incong- recombinant sequences, especially if it detection is challenging and often subject
ruence between phylogenies reconstructed occurs repeatedly, and differentially, over to failure. First, it is well established that
from genes with different histories of the course of speciation.12 Each recom- recombination detection programs per-
transfer, including of course no transfer binant gene, if analyzed as a whole, form poorly when sequence divergence
at all. Finding and examining phylogene- might or might not reflect the true is low.18-21 Unfortunately, plant mito-
tically atypical genes has become a stand- evolutionary history of either or both chondrial genomes, which collectively
ardtaskinHGTstudies.5-7Incaseswhere parental sequences. When parental constitute a premiere model system for
an entire gene has been transferred, sequences contribute differentially to the eukaryotic HGT studies,4,22 usually have
without the complication of recombina- number of informative characters in a very lowratesofnucleotidesubstitution.23
tion/conversion with a native homolog, recombinant sequence, this sequence will Second, gene conversion often involves
the donor lineage can in principle be tend to resemble the parental sequence very short tracts of DNA,13,14 which can
identified as the nearest phylogenetic that contributes more informative char- make recombination detection very diffi-
neighbor.7-9 Gene conversion enters the acters (e.g., refs. 15 and 16), whereas cult. For instance, ten previously pub-
picture either during the act of gene when parental sequences contribute sim- lished recombinant regions between plant
transfer, when transiently-present foreign ilar numbers of informative characters, mitochondrialand chloroplast genes range
DNA directly converts (replaces) part of a the recombinant will potentially be quite in length from only 14 to 79 nucleo-
nativelocus10,11or,afterduplicativeHGT, different from both parental sequences, tides.24,25 Third, existing recombination
via potentially ongoing gene conversion depending of course on the degree of detection programs are generally designed
*Correspondenceto:WeilongHao;Email:[email protected]
Submitted:10/31/11;Revised:12/11/11;Accepted:12/13/11
http://dx.doi.org/10.4161/mge.19030
256 MobileGeneticElements Volume1Issue4
LETTERTOTHEEDITOR
to identify a single or only a small withinTernstroemiapossessesadifferenti- related mosaic genes and emphasizes that
numberofrecombinationbreakpoints.26,27 ally mosaic atp1 gene, each with multiple this position provides little or no reliable
Intricate gene conversion during the pro- (four to five) foreign regions interspersed information on the nature of the gene’s
cess of duplicative HGT and differential with native regions. In the one atp1 parental sequences.
gene conversion (DH-DC) can, however, phylogeny presented in reference 12, the The only other topological difference
lead to mosaic gene structures, with mosaicTernstroemiageneswereallplaced among all five atp1 trees (Fig.2B–F)
multiple foreign regions interspersed with within the Eriaceae, in a paraphyletic involves Chamaedaphne, which was
native regions on a fine scale. relationship with respect to Vaccinium. weakly placed (41% bootstrap support)
We recently reported such mosaicism To better understand how mosaic within Vaccinium when all mosaic genes
in mitochondrial atp1 and matR genes genes affect phylogeny reconstruction, we wereincluded(Fig.2B),butwasplacedas
belonging to different groups of flowering sequenced the mitochondrial atp1 gene sister (with 68–92% support) to a mono-
plants (angiosperms). We show that these of Chamaedaphne calyculata, a close rela- phyletic Vaccinium in the other four gene
mosaic genes largely escaped detection by tive of Vaccinium,28 using the same set of trees. This result raises the possibility that
recombination-detection programs and primers and method as in reference 12, the inclusion of mosaic sequences in
were recognizable only by direct visual and employed it together with varying phylogenetic analyses can affect not only
inspectionofDNAsequencealignments.12 subsets of previously sequenced Ericales theplacementofrelatedmosaicsequences,
In this report, we explore the effects of atp1 genes in maximum likelihood phylo- butalsotheplacementofapparentlynative
chimeric sequences on phylogeny recon- genetic analyses. The Chamaedaphne atp1 sequences.
struction by conducting phylogenetic sequencewasdepositedinGenBankunder Phylogenetic analysis of simulated
©analys es 2on sim0ulated1sequen2ces an dLon aaccessnion nudmbereJN808s446. CBonsistenit ochimseric scequenicese. Wenused scimulaetion .
an augmented set of the atp1 sequences with our recent study,12 and in contrast studies (conducted using Seq-Gen29) to
analyzed in reference 12. to organismal phylogeny (Fig.2A), in an further explore the effects of chimeric
analysis that included all relevant genes, sequences on phylogeny reconstruction.
Results the three types of mosaic atp1 genes The following simulation parameters
in Ternstroemia formed a paraphyletic were chosen to be the same as those
Phylogenetic analysis of naturally-occur- assemblage, with T. fragrans sister to the used in the above analysis of atp1
Do not distribute.
ring mosaic genes. In arecent study,12we Vaccinium/Chamaedaphneclade,theT-glj sequences: (1) sequence length, 1200
reportedthepresenceofthreedifferentially cladethemostdistantfromtheVaccinium/ nucleotides; (2) substitution model, GTR;
mosaic types of mitochondrial atp1 genes Chamaedaphne clade and the T-ips clade (3)gammashapeparameter,0.218;(4)pro-
in the angiosperm genus Ternstroemia in an intermediate position (Fig.2B). portionofinvariantsites:0.371;(5)nucleo-
(Pentaphylaceae, Ericales) and concluded Remarkably, when only one type of tide frequencies, 0.271 (A), 0.207 (C),
that they arose via DH-DC, with the mosaic atp1 gene was included in a given 0.261 (G) and 0.261 (T); and (6) GTR
blueberrygenusVaccinium(Ericaceae)the analysis, each of the three types fell relativerateparameters,A,-.C=0.818,
best candidate to be the donor group in a different phylogenetic position A , -.G = 1.938,A, - .T= 0.244,
in the initiating HGT event. As shown (Fig.2C–E). This shows that the phylo- C , - . G = 0.884,C , - . T = 2.219
in Figure1 (adapted from Fig.2A of genetic position of a mosaic gene can vary and G , - . T = 1.000. All but the first
ref. 12), each of the three major clades depending on the inclusion of additional, of these parameters are based on PhyML30
Figure1.Threetypesofmosaicmitochondrialatp1genesinTernstroemia(adaptedfromref.12).Themulti-coloredboxesrepresentatp1genesofthe
threesubcladeswithinTernstroemia.Blackverticallinesrepresentthe38nucleotidepositionsinferred12tohavedifferedbetweendonorandrecipient
atp1genesatthetimeofatp1transferfromVacciniumtoacommonancestorofTernstroemia.Linesatthetopoftheboxesandredshadingindicate
sitesandregions,respectively,ofputativelyforeign,Vacciniumancestry,whilebottomlinesandblueshadingrepresentnativesitesandregions.White
linescenteredwithintheboxesrepresenttheonlytwositesthatotherwisedifferwithintheTernstroemiaclade.“T-ips”referstotheTernstroemia
subcladecontainingT.impressa,T.peduncularisandT.stahlii)and“T-glj”tothesubcladecontainingT.gymnanthera,T.longipesandT.japonica(seealso
Fig.2A).
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© 2012 Landes Bioscience.
Figure2.PhylogeneticaDnalysisoofmosai cmnitochonodrialattp1ge neds.(A)Chironsogramtshowringiorgabnismalurelationtshipseandd.ivergencetimesofrelevant
taxabelongingtotheEricales.Asdescribedinreference12,thechronogramwasconstructedbytheBEASTprogram43usingaEuryareferencefossil
calibrationof86Myrago.44(B-F)Maximumlikelihoodphylogeniesofmitochondrialatp1genesfromthetaxashownin(A),withtheseanalysesvaryingas
towhichmembersofTernstroemia(showninred),whoseatp1geneisdifferentiallymosaic,wereincluded.RAxML32version7.0.4wasusedtoconstruct
allphylogenieswithaGTR+C+Isubstitutionmodel.Atotalof1000bootstrapiterationswereperformed,withallbootstrapvalues$50%shown
onthetrees.PhylogenieswererootedusingFouquieria,MarcgraviaandPentameristaasunshownoutgroups(hencethestubbranchatthebase
ofeachgenetree).
estimates derived from the mitochondrial varied the parental proportions that com- The phylogenetic position of the 50:50
atp1alignment shown inFigureS1, except prise the chimeric sequence(s) and the chimeric sequence also varied substanti-
with the mosaic Ternstroemia genes numberofchimericsequencesincludedin ally depending on whether it was the
excluded(as in Fig.2F) because recombin- a given analysis. In analyses with a single only chimeric sequence in the analysis
ant genes have been shown to alter the chimeric sequence, this sequence grouped (Fig.3D) or whether the 30:70 and/or
estimation of substitution rate heterogen- with 100% bootstrap support with its 10:90 sequences were also included
eity.31Theremainingsimulationparameters majority parental sequence when the (Fig.3E–G). Inclusion of the 30:70
were independent of the atp1 data and parental ratio was 10:90 (i.e., when the sequence, either with (Fig.3E) or without
include the number of sequences, their chimeric sequence consisted of 10% (Fig.3F) the 10:90, “pulled” the 50:50
topology, relative branchlengths and abso- of sequence 9 and 90% of sequence 1; from the base of the tree to its periphery,
lute amount of divergence (Fig.3A). For Fig.3B).Thesametopologywasobtained together with the 30:70 and parental
simplicity, only one recombination break- with the30:70chimera(Fig.3C),butthe sequence 1 (and with the 10:90 when
point was allowed in each chimeric bootstrap value dropped to 92. When the included) and with strong support (96%
sequence, with these chimerics constructed chimera was 50:50 (Fig.3D), it went to and 92%, respectively). This peripheral
tocontainvaryingproportions(from50:50 the base of the tree, in between the two attraction was more subdued when the
to 10:90) of two of the 16 “parental” main clades of simulated sequences, and 50:50waspairedwiththe10:90(Fig.3G)
sequences generated by the simulations. with bootstrap support reduced along as opposed to the 30:70 (Fig.3F), pre-
The16purely-simulatedsequencestogether the branches leading to both parental sumably because of the greater proportion
with the artificially constructed chimeric sequences. These results thus show that of sequence length shared by the 30:70
sequencewereusedinphylogeneticanalyses the phylogenetic position of chimeric and50:50(80%)relativetothe10:90and
performedusingRAxMLversion7.0.4.32 genes can vary substantially as the propor- 50:50 (60%). Also, there is evidence for a
Two sets of simulation analyses were tion of parental sequences that comprise mutual attraction between the 10:90 and
performed. In the first set (Fig.3), we the chimerics varies. 50:50 (but not between the 30:70 and
258 MobileGeneticElements Volume1Issue4
© 2012 Landes Bioscience.
Figure3.Variablephylogeneticplacementofchimericgenesdemonstratedbysimulations.Artificialsequencesweresimulatedasdescribedinthetext.
Chimericsequencesweregeneratedbycombiningthe5’and3’portionsofsequences1and9,respectively(bothcircledinred),withdifferentlength
Do not distribute.
ratios(10:90,30:70or50:50)ofthetwoparentalsequences.Onethousandtree-buildingiterationswereperformed.Thetreeshownineachpanelis
based(forcomputationalease)ontheconcatenatedsequencesofthefirst100iterations,whilethebootstrapsupportvaluesarefromall1000trees.
Allbootstrapvaluesare$95%exceptforthoseshown.
50:50), in that the bootstrap support for the 50:50 chimeric in the single-chimeric simulated sequences become more diver-
the10:90groupingwithparentalsequence analysis of Figure3D resulted in the loss gent, the parental sequences show an
1 was reduced from 100% (Fig.3B) to of a molecular clock among the non- increased and pronounced, tendency to
only 54% (Fig.3G). These simulation recombinant sequences in this analysis, be attracted toward the base of the tree
results are consistent with the empirical withthebranchleadingtothe(1–4)clade by the chimeric gene. Also, the branch
results (Fig.2) in showing that the only 60% of the length leading to the leading to the chimeric sequence becomes
phylogenetic position of a chimeric gene (5–8) clade and the branch leading to the increasingly short, approaching zero in
can vary substantially when different (9–12) clade only 58% of the length Figure4C and D. It is important to note
additional chimeric genes are sampled. leading to the (13–16) clade. There are that this effect is not simply the result
We also found that chimeric genes can consistently two additional—albeit much of there being increasingly more informa-
perturb phylogenetic analysis by pro- less pronounced—sets of branch length tive characters from Figure4A–D. In
ducing branch length bias. First, certain differencesinthesixtrees(Fig.3B,Cand analyses with 5 (cid:1) or 10 (cid:1) divergence
chimeric genes were directly associated E–H) in which one or more chimeric (data not shown), but only 1/10th the
with elongated branch lengths. In the sequences are sister to sequence 1. sequence length (120 nucleotides rather
single-chimeric analyses, the 10:90 chi- The second set of simulations showed than the 1200 in the simulations shown
mera had a notably longer branch length thatchimericsequencescanalsoconfound in Figure4), the topology and bootstrap
thansequence1(Fig.3B),whilethe30:70 phylogenetic analysis by altering the values were essentially identical with those
branch length was even longer (Fig.3C), placement of non-recombinant (native) in Figure4C and D, respectively, with
with the (homoplasious) substitutions sequences. In these simulations (Fig.4), these being substantially different from
contributed by the 30% of the chimeric wevariedtheabsoluteamountofsequence those in Figure4A and B. The different
sequence originating from sequence 9 divergence across the tree, with the 50:50 topologies shown in Figure4 must there-
presumably responsible for this greatly sequence the only chimeric sequence in foreresultfromdeterministiceffectsarising
extended branch length. Similar results each analysis. Figure4A shows the same from the varying levels of divergence in
were obtained in Figure3E–H, where tree as Figure3D, while Figure4B–D these trees. These simulations thus show
multiplechimericsequenceswereincluded has expanded divergence by a factor of thatinclusionofchimericsequencescandis-
in each analysis. Second, the presence of 2 (cid:1), 5(cid:1) and 10 (cid:1) , respectively. As the tort the branching pattern of nonchimeric,
www.landesbioscience.com MobileGeneticElements 259
Figure4.Chimericsequencesincreasinglydisruptnative-sequencetopologiesasdivergenceincreases.(A)Thesametreeasshownin Figure3D.
(B–D)Maximumlikelihoodanalysisofthesamesimulatedsequences,butwithincreasingbranch-lengthscalesacrossthesetofsequences:
(B)2(cid:1)thescalein(A);(C)5(cid:1);and(D)10(cid:1).Onethousandtree-buildingiterationswereperformed.Thetreeshownineachpanelisbased
(forcomputationalease)ontheconcatenatedsequencesofthefirst100iterations,whilethebootstrapsupportvaluesarefromall1,000trees.
Allbootstrapvaluesare$95%exceptforthoseshown.
© 2012 Landes Bioscience.
native sequences and that the extent of Streptococcus pneumoniae,35,36 Helicobacter analysis, nor did they show that chimeric
this distortion varies directly with the pylori37 and Wolbachia38 have been found sequences can, under certain conditions,
absolute level of sequence divergence. tobesorecombinogenicthatscientistshave substantiallyalterthephylogeneticbehavior
resorted to using multiple loci (e.g., multi- of native sequences. Further simulation
Discussion locus sequence typing39) as opposed to a studies on the effects of recombination on
singlelocustoidentifyclones.Surprisingly, phylogenetic inference would therefore
Do not distribute.
The analyses reported in this study show however, the phenomenon of HGT tur- appeartobecalledfor.
that the inclusion in phylogenetic analyses bulence has never been explicitly addressed Recognitionoftheremarkablefrequency
of chimeric sequences arising from HGT in the bacterial literature. One reason for andextentofhorizontalgenetransfer,andits
and gene conversion can produce a variety thisisthatthesestudieshavemainlyfocused often great evolutionary importance, is
of spurious phylogenetic results. These on minimizing the effect of recombination arguably the greatest accomplishment of
include the misplacement of both chimeric and thereby inferring accurate evolutionary the past 15 years of comparative genomics
and native sequences, as well as branch relationships,oronquantifyingthenumber research. Because HGT isso common and
length distortions. Accordingly, we intro- of recombinant genes, rather than actually important,recognizingandproperlydealing
duce the term “HGT turbulence” as a exploring the topological alterations caused withHGTturbulenceislikewiseimportant.
general moniker for this category of phy- by HGT turbulence. Also, the precise This is so not only because of the obvious
logenetic artifacts. Mutually reinforcing origins of horizontally transferred genes (or needforobtainingaccurateestimatesofgene
evidenceforthesetypesofHGTturbulence gene fragments) in bacterial genomes can and species phylogeny, but also because
wasapparentinthephylogeneticanalysesof be extremely difficult to recover, especially otherwisetoomanycasesofchimericHGT,
both simulated sequences and a naturally when transfer and/or subsequent recom- including complex situations involving
occurring set of native and chimeric binationhaveoccurredonafinescale. DH-DC,willcontinuetogooverlooked.
mitochondrial sequences, with the simula- Several other studies17,31,40-42 have used
tions providing greater opportunity to recombinant sequences in phylogenetic Acknowledgments
crystallize and illustrate specific sets of simulations, but most of these have We thank the two reviewers for critical
sequence interactions and consequences. It focused on the issue of whether recombi- reading of the manuscript; the Kew
isalso important to realize that while these nants are detectable and/or how to detect DNA Bank (Royal Botanic Gardens;
simulations were framed and presented in them. Perhaps most relevant to our Kew, UK) for providing the Chama-
the context of HGT, their results apply study is the 2002 study by Posada and edaphne calyculata DNA and Y. Zheng
equallywelltoconversionbetweenparalogs Crandall,17 which also explored the rela- for technical assistance. W.H. was sup-
arisingfrominternalgeneduplicationasto tionship between the location of recombi- portedbystartupfundsfromWayneState
xenologsarisingfromHGT. nation breakpoints and the phylogenetic University. J.D.P. was supported by
HGT turbulence is probably relatively placement of recombinant sequences, National Institutes of Health Grant R01-
commoninbacteria,1,2giventheprevalence reachingsimilarconclusiontooursonthis GM-70612 and by the METACyt
ofHGTandrecombinationduringbacterial point. However, none of these studies Initiative of Indiana University, funded
genome evolution. For example, such exploredtheeffectsofcombiningmultiple, in part through a major grant from the
diversebacteriaasNeisseriameningitidis,33,34 related chimeric sequences in the same Lilly Endowment, Inc.
260 MobileGeneticElements Volume1Issue4
Supplemental Materials
Supplemental materials can be found at:
www.landesbioscience.com/journals/mge/
article/19030
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