Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes
Gene duplication followed by neo- or sub-functionalization deeply impacts the evolution of protein families and is regarded as the main source of adaptive functional novelty in eukaryotes. While there is ample evidence of adaptive gene duplication in prokaryotes, it is not clear whether duplication outweighs the contribution of horizontal gene transfer in the expansion of protein families. We analyzed closely related prokaryote strains or species with small genomes (Helicobacter, Neisseria, Streptococcus, Sulfolobus), average-sized genomes (Bacillus, Enterobacteriaceae), and large genomes (Pseudomonas, Bradyrhizobiaceae) to untangle the effects of duplication and horizontal transfer. After removing the effects of transposable elements and phages, we show that the vast majority of expansions of protein families are due to transfer, even among large genomes. Transferred genes—xenologs—persist longer in prokaryotic lineages possibly due to a higher/longer adaptive role. On the other hand, duplicated genes—paralogs—are expressed more, and, when persistent, they evolve slower. This suggests that gene transfer and gene duplication have very different roles in shaping the evolution of biological systems: transfer allows the acquisition of new functions and duplication leads to higher gene dosage. Accordingly, we show that paralogs share most protein–protein interactions and genetic regulators, whereas xenologs share very few of them. Prokaryotes invented most of life's biochemical diversity. Therefore, the study of the evolution of biology systems should explicitly account for the predominant role of horizontal gene transfer in the diversification of protein families.
Vyšlo v časopise:
Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes. PLoS Genet 7(1): e32767. doi:10.1371/journal.pgen.1001284
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001284
Souhrn
Gene duplication followed by neo- or sub-functionalization deeply impacts the evolution of protein families and is regarded as the main source of adaptive functional novelty in eukaryotes. While there is ample evidence of adaptive gene duplication in prokaryotes, it is not clear whether duplication outweighs the contribution of horizontal gene transfer in the expansion of protein families. We analyzed closely related prokaryote strains or species with small genomes (Helicobacter, Neisseria, Streptococcus, Sulfolobus), average-sized genomes (Bacillus, Enterobacteriaceae), and large genomes (Pseudomonas, Bradyrhizobiaceae) to untangle the effects of duplication and horizontal transfer. After removing the effects of transposable elements and phages, we show that the vast majority of expansions of protein families are due to transfer, even among large genomes. Transferred genes—xenologs—persist longer in prokaryotic lineages possibly due to a higher/longer adaptive role. On the other hand, duplicated genes—paralogs—are expressed more, and, when persistent, they evolve slower. This suggests that gene transfer and gene duplication have very different roles in shaping the evolution of biological systems: transfer allows the acquisition of new functions and duplication leads to higher gene dosage. Accordingly, we show that paralogs share most protein–protein interactions and genetic regulators, whereas xenologs share very few of them. Prokaryotes invented most of life's biochemical diversity. Therefore, the study of the evolution of biology systems should explicitly account for the predominant role of horizontal gene transfer in the diversification of protein families.
Zdroje
1. McCutcheonJP
McDonaldBR
MoranNA
2009
Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont.
PLoS Genet
5
e1000565
doi:10.1371/journal.pgen.1000565
2. SchneikerS
PerlovaO
KaiserO
GerthK
AliciA
2007
Complete genome sequence of the myxobacterium Sorangium cellulosum.
Nat Biotechnol
25
1281
1289
3. PasekS
RislerJL
BrezellecP
2006
The role of domain redundancy in genetic robustness against null mutations.
J Mol Biol
362
184
191
4. Pereira-LealJB
LevyED
KampC
TeichmannSA
2007
Evolution of protein complexes by duplication of homomeric interactions.
Genome Biol
8
R51
5. WagnerA
2008
Gene duplications, robustness and evolutionary innovations.
Bioessays
30
367
373
6. FrancinoMP
2005
An adaptive radiation model for the origin of new gene functions.
Nat Genet
37
573
577
7. KugelbergE
KofoidE
ReamsAB
AnderssonDI
RothJR
2006
Multiple pathways of selected gene amplification during adaptive mutation.
Proc Natl Acad Sci U S A
103
17319
17324
8. AnderssonDI
HughesD
2009
Gene amplification and adaptive evolution in bacteria.
Annu Rev Genet
43
167
195
9. ConantGC
WolfeKH
2008
Turning a hobby into a job: how duplicated genes find new functions.
Nat Rev Genet
9
938
950
10. RothC
RastogiS
ArvestadL
DittmarK
LightS
2007
Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms.
J Exp Zoolog B Mol Dev Evol
308
58
73
11. DemuthJP
HahnMW
2009
The life and death of gene families.
Bioessays
31
29
39
12. InnanH
KondrashovF
2010
The evolution of gene duplications: classifying and distinguishing between models.
Nat Rev Genet
11
97
108
13. AlmE
HuangK
ArkinA
2006
The evolution of two-component systems in bacteria reveals different strategies for niche adaptation.
PLoS Comput Biol
2
e143
doi:10.1371/journal.pcbi.0020143
14. SerresMH
KerrAR
McCormackTJ
RileyM
2009
Evolution by leaps: gene duplication in bacteria.
Biol Direct
4
46
15. TreangenTJ
AbrahamAL
TouchonM
RochaEP
2009
Genesis, effects and fates of repeats in prokaryotic genomes.
FEMS Microbiol Rev
33
539
571
16. ChoNH
KimHR
LeeJH
KimSY
KimJ
2007
The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host-cell interaction genes.
Proc Natl Acad Sci U S A
104
7981
7986
17. GoldmanBS
NiermanWC
KaiserD
SlaterSC
DurkinAS
2006
Evolution of sensory complexity recorded in a myxobacterial genome.
Proc Natl Acad Sci U S A
103
15200
15205
18. McLeodMP
WarrenRL
HsiaoWW
ArakiN
MyhreM
2006
The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse.
Proc Natl Acad Sci U S A
103
15582
15587
19. LindroosH
VinnereO
MiraA
RepsilberD
NaslundK
2006
Genome rearrangements, deletions, and amplifications in the natural population of Bartonella henselae.
J Bacteriol
188
7426
7439
20. EvlampievK
IsambertH
2008
Conservation and topology of protein interaction networks under duplication-divergence evolution.
Proc Natl Acad Sci U S A
105
9863
9868
21. TeichmannSA
BabuMM
2004
Gene regulatory network growth by duplication.
Nat Genet
36
492
496
22. OchmanH
LawrenceJG
GroismanEA
2000
Lateral gene transfer and the nature of bacterial innovation.
Nature
405
299
304
23. LeratE
DaubinV
OchmanH
MoranNA
2005
Evolutionary origins of genomic repertoires in bacteria.
PLoS Biol
3
e130
doi:10.1371/journal.pbio.0030130
24. GogartenJP
DoolittleWF
LawrenceJG
2002
Prokaryotic evolution in light of gene transfer.
Mol Biol Evol
19
2226
2238
25. TettelinH
RileyD
CattutoC
MediniD
2008
Comparative genomics: the bacterial pan-genome.
Curr Opin Microbiol
11
472
477
26. KuninV
OuzounisCA
2003
The balance of driving forces during genome evolution in prokaryotes.
Genome Res
13
1589
1594
27. ZhaxybayevaO
GogartenJP
CharleboisRL
DoolittleWF
PapkeRT
2006
Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events.
Genome Res
16
1099
1108
28. DaganT
Artzy-RandrupY
MartinW
2008
Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution.
Proc Natl Acad Sci U S A
105
10039
10044
29. SnelB
BorkP
HuynenMA
2002
Genomes in flux: the evolution of archaeal and proteobacterial gene content.
Genome Res
12
17
25
30. HooperSD
BergOG
2003
Duplication is more common among laterally transferred genes than among indigenous genes.
Genome Biol
4
R48
31. GeversD
VandepoeleK
SimillonC
Van de PeerY
2004
Gene duplication and biased functional retention of paralogs in bacterial genomes.
Trends Microbiol
12
148
154
32. PushkerR
MiraA
Rodriguez-ValeraF
2004
Comparative genomics of gene-family size in closely related bacteria.
Genome Biol
5
R27
33. PagelM
MeadeA
BarkerD
2004
Bayesian estimation of ancestral character states on phylogenies.
Syst Biol
53
673
684
34. WagnerA
2006
Periodic extinctions of transposable elements in bacterial lineages: evidence from intragenomic variation in multiple genomes.
Mol Biol Evol
23
723
733
35. TouchonM
RochaEP
2007
Causes of insertion sequences abundance in prokaryotic genomes.
Mol Biol Evol
24
969
981
36. van PasselMW
MarriPR
OchmanH
2008
The emergence and fate of horizontally acquired genes in Escherichia coli.
PLoS Comput Biol
4
e1000059
doi:10.1371/journal.pcbi.1000059
37. RochaEP
2008
Evolutionary patterns in prokaryotic genomes.
Curr Opin Microbiol
11
454
460
38. RomeroD
PalaciosR
1997
Gene amplification and genomic plasticity in prokaryotes.
Annu Rev Genet
31
91
111
39. AchazG
RochaEPC
NetterP
CoissacE
2002
Origin and fate of repeats in bacteria.
Nucleic Acids Res
30
2987
2994
40. Howell-AdamsB
SeifertHS
2000
Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation.
Mol Microbiol
37
1146
1158
41. ArasRA
KangJ
TschumiAI
HarasakiY
BlaserMJ
2003
Extensive repetitive DNA facilitates prokaryotic genome plasticity.
Proc Natl Acad Sci U S A
100
13579
13584
42. FalushD
KraftC
TaylorNS
CorreaP
FoxJG
2001
Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age.
Proc Natl Acad Sci U S A
98
15056
15061
43. FeilEJ
HolmesEC
BessenDE
ChanMS
DayNP
2001
Recombination within natural populations of pathogenic bacteria: short- term empirical estimates and long-term phylogenetic consequences.
Proc Natl Acad Sci U S A
98
182
187
44. SharpPM
LiWH
1987
The codon Adaptation Index - a measure of directional synonymous codon usage bias, and its potential applications.
Nucleic Acids Res
15
1281
1295
45. MasudaT
SaitoN
TomitaM
IshihamaY
2009
Unbiased quantitation of Escherichia coli membrane proteome using phase transfer surfactants.
Mol Cell Proteomics
8
2770
2777
46. ParmleyJL
HurstLD
2007
How common are intragene windows with KA>KS owing to purifying selection on synonymous mutations?
J Mol Evol
64
646
655
47. LawrenceJG
OchmanH
1997
Amelioration of bacterial genomes: rates of change and exchange.
J Mol Evol
44
383
397
48. VernikosGS
ThomsonNR
ParkhillJ
2007
Genetic flux over time in the Salmonella lineage.
Genome Biol
8
R100
49. RochaEPC
DanchinA
2004
An analysis of determinants of protein substitution rates in Bacteria.
Mol Biol Evol
21
108
116
50. HuP
JangaSC
BabuM
Diaz-MejiaJJ
ButlandG
2009
Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins.
PLoS Biol
7
e96
doi:10.1371/journal.pbio.1000096
51. Martinez-NunezMA
Perez-RuedaE
Gutierrez-RiosRM
MerinoE
2010
New insights into the regulatory networks of paralogous genes in bacteria.
Microbiology
156
14
22
52. PriceMN
DehalPS
ArkinAP
2008
Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli.
Genome Biol
9
R4
53. LercherMJ
PalC
2008
Integration of horizontally transferred genes into regulatory interaction networks takes many million years.
Mol Biol Evol
25
559
567
54. CorderoOX
HogewegP
2009
The impact of long-distance horizontal gene transfer on prokaryotic genome size.
Proc Natl Acad Sci U S A
106
21748
21753
55. SorekR
ZhuY
CreeveyCJ
FrancinoMP
BorkP
2007
Genome-wide experimental determination of barriers to horizontal gene transfer.
Science
318
1449
1452
56. VernikosG
ThomsonN
ParkhillJ
2007
Genetic flux over time in the Salmonella lineage.
Genome Biology
8
R100
57. IsambertH
SteinRR
2009
On the need for widespread horizontal gene transfers under genome size constraint.
Biol Direct
4
28
58. RochaEPC
2006
Inference and Analysis of the Relative Stability of Bacterial Chromosomes.
Mol Biol Evol
23
513
522
59. PalC
PappB
LercherMJ
2005
Adaptive evolution of bacterial metabolic networks by horizontal gene transfer.
Nat Genet
37
1372
1375
60. OchmanH
LiuR
RochaEP
2007
Erosion of interaction networks in reduced and degraded genomes.
J Exp Zoolog B Mol Dev Evol
308
97
103
61. WellnerA
LurieMN
GophnaU
2007
Complexity, connectivity, and duplicability as barriers to lateral gene transfer.
Genome Biol
8
R156
62. KeelingPJ
PalmerJD
2008
Horizontal gene transfer in eukaryotic evolution.
Nat Rev Genet
9
605
618
63. DerelleE
FerrazC
RombautsS
RouzeP
WordenAZ
2006
Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features.
Proc Natl Acad Sci U S A
103
11647
11652
64. BowlerC
AllenAE
BadgerJH
GrimwoodJ
JabbariK
2008
The Phaeodactylum genome reveals the evolutionary history of diatom genomes.
Nature
456
239
244
65. AltschulSF
GishW
MillerW
MyersEW
LipmanDJ
1990
Basic local alignment search tool.
J Mol Biol
215
403
410
66. EnrightAJ
Van DongenS
OuzounisCA
2002
An efficient algorithm for large-scale detection of protein families.
Nucleic Acids Res
30
1575
1584
67. SiguierP
PerochonJ
LestradeL
MahillonJ
ChandlerM
2006
ISfinder: the reference centre for bacterial insertion sequences.
Nucleic Acids Res
34
D32
36
68. FoutsDE
2006
Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences.
Nucleic Acids Res
34
5839
5851
69. TreangenTJ
DarlingAE
AchazG
RaganMA
MesseguerX
2009
A novel heuristic for local multiple alignment of interspersed DNA repeats.
IEEE/ACM Trans Comput Biol BioInf
6
180
189
70. LiL
StoeckertCJJr
RoosDS
2003
OrthoMCL: identification of ortholog groups for eukaryotic genomes.
Genome Res
13
2178
2189
71. RochaEP
TouchonM
FeilEJ
2006
Similar compositional biases are caused by very different mutational effects.
Genome Res
16
1537
1547
72. AzadRK
LawrenceJG
2007
Detecting laterally transferred genes: use of entropic clustering methods and genome position.
Nucleic Acids Res
35
4629
4639
73. EdgarRC
2004
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
Nucleic Acids Res
32
1792
1797
74. SchmidtHA
StrimmerK
VingronM
von HaeselerA
2002
TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
Bioinformatics
18
502
504
75. GascuelO
1997
BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data.
Mol Biol Evol
14
685
695
76. YangZ
1997
PAML: a program package for phylogenetic analysis by maximum likelihood.
CABIOS
13
555
556
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