journal article Open Access Oct 01, 2021

Gene Duplications Are At Least 50 Times Less Frequent than Gene Transfers in Prokaryotic Genomes

View at Publisher Save 10.1093/gbe/evab224
Abstract
AbstractThe contribution of gene duplications to the evolution of eukaryotic genomes is well studied. By contrast, studies of gene duplications in prokaryotes are scarce and generally limited to a handful of genes or careful analysis of a few prokaryotic lineages. Systematic broad-scale studies of prokaryotic genomes that sample available data are lacking, leaving gaps in our understanding of the contribution of gene duplications as a source of genetic novelty in the prokaryotic world. Here, we report conservative and robust estimates for the frequency of recent gene duplications within prokaryotic genomes relative to recent lateral gene transfer (LGT), as mechanisms to generate multiple copies of related sequences in the same genome. We obtain our estimates by focusing on evolutionarily recent events among 5,655 prokaryotic genomes, thereby avoiding vagaries of deep phylogenetic inference and confounding effects of ancient events and differential loss. We find that recent, genome-specific gene duplications are at least 50 times less frequent and probably 100 times less frequent than recent, genome-specific, gene acquisitions via LGT. The frequency of gene duplications varies across lineages and functional categories. The findings improve our understanding of genome evolution in prokaryotes and have far-reaching implications for evolutionary models that entail LGT to gene duplications ratio as a parameter.
Topics

No keywords indexed for this article. Browse by subject →

References
54
[1]
Basic local alignment search tool

Stephen F. Altschul, Warren Gish, Webb Miller et al.

Journal of Molecular Biology 1990 10.1016/s0022-2836(05)80360-2
[2]
Andersson "Evolution of new functions de novo and from preexisting genes" Cold Spring Harb Perspect Biol (2015) 10.1101/cshperspect.a017996
[3]
Arakawa "No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade" Proc Natl Acad Sci U S A (2016) 10.1073/pnas.1602711113
[4]
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

Yoav Benjamini, Yosef Hochberg

Journal of the Royal Statistical Society Series B:... 1995 10.1111/j.2517-6161.1995.tb02031.x
[5]
Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria

P M Bennett

British Journal of Pharmacology 2008 10.1038/sj.bjp.0707607
[6]
Bratlie "Gene duplications in prokaryotes can be associated with environmental adaptation" BMC Genomics (2010) 10.1186/1471-2164-11-588
[7]
Chojnacki "Programmatic access to bioinformatics tools from EMBL-EBI update: 2017" Nucleic Acids Res (2017) 10.1093/nar/gkx273
[8]
Cohen "The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer" Mol Biol Evol (2011) 10.1093/molbev/msq333
[9]
Coissac "A comparative study of duplications in bacteria and eukaryotes: the importance of telomeres" Mol Biol Evol (1997) 10.1093/oxfordjournals.molbev.a025712
[10]
Coleman "A rooted phylogeny resolves early bacterial evolution" Science (2021) 10.1126/science.abe0511
[11]
Curcio "The outs and ins of transposition: from MU to kangaroo" Nat Rev Mol Cell Biol (2003) 10.1038/nrm1241
[12]
Dagan "Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution" Proc Natl Acad Sci U S A (2008) 10.1073/pnas.0800679105
[13]
Dagan "Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution" Proc Natl Acad Sci U S A (2007) 10.1073/pnas.0606318104
[14]
Davis "Genomes of the class Erysipelotrichia clarify the firmicute origin of the class Mollicutes" Int J Syst Evol Microbiol (2013) 10.1099/ijs.0.048983-0
[15]
Doyon "Models, algorithms and programs for phylogeny reconciliation" Brief Bioinform (2011) 10.1093/bib/bbr045
[16]
An efficient algorithm for large-scale detection of protein families

A. J. Enright

Nucleic Acids Research 2002 10.1093/nar/30.7.1575
[17]
Garg "Anomalous phylogenetic behaviour of ribosomal proteins in metagenome-assembled asgard archaea" Genome Biol Evol (2021) 10.1093/gbe/evaa238
[18]
Gautreau "PPanGGOLiN: depitcting microbial diversity via partioned pangenome graph" PLoS Comput Biol (2020) 10.1371/journal.pcbi.1007732
[19]
Gevers "Gene duplication and biased functional retention of paralogs in bacterial genomes" Trends Microbiol (2004) 10.1016/j.tim.2004.02.007
[20]
Goodman "Globin evolution was apparently very rapid in early vertebrates: a reasonable case against the rate-constancy hypothesis" J Mol Evol (1981) 10.1007/bf01732683
[21]
KEGG as a reference resource for gene and protein annotation

Minoru Kanehisa, Yoko Sato, Masayuki Kawashima et al.

Nucleic Acids Research 2016 10.1093/nar/gkv1070
[23]
Lane "The energetics of genome complexity" Nature (2010) 10.1038/nature09486
[24]
Lerat "Evolutionary origins of genomic repertoires in bacteria" PLoS Biol (2005) 10.1371/journal.pbio.0030130
[25]
Li "Detection of gene duplications and block duplications in eukaryotic genomes" J Struct Funct Genomics (2003) 10.1023/a:1022644628861
[26]
The evolutionary demography of duplicate genes

Michael Lynch, John S. Conery

Journal of Structural and Functional Genomics 2003 10.1023/a:1022696612931
[27]
McInerney "Why prokaryotes have pangenomes" Nat Microbiol (2017) 10.1038/nmicrobiol.2017.40
[28]
Méheust "Hundreds of novel composite genes and chimeric genes with bacterial origins contributed to haloarchaeal evolution" Genome Biol (2018) 10.1186/s13059-018-1454-9
[29]
Nagies "A spectrum of verticality across genes" PLoS Genet (2020) 10.1371/journal.pgen.1009200
[30]
Nelson-Sathi "Origins of major archaeal clades correspond to gene acquisitions from bacteria" Nature (2015) 10.1038/nature13805
[31]
Nunes "Evolution, phylogeny, and molecular epidemiology of Chlamydia" Infect Genet Evol (2014) 10.1016/j.meegid.2014.01.029
[32]
Lateral gene transfer and the nature of bacterial innovation

Howard Ochman, Jeffrey G. Lawrence, Eduardo A. Groisman

Nature 2000 10.1038/35012500
[33]
Evolution by Gene Duplication

Susumu Ohno

1970 10.1007/978-3-642-86659-3
[34]
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation

Nuala A. O'Leary, Mathew W. Wright, J. Rodney Brister et al.

Nucleic Acids Research 2016 10.1093/nar/gkv1189
[35]
Popa "Trends and barriers to lateral gene transfer in prokaryotes" Curr Opin Microbiol (2011) 10.1016/j.mib.2011.07.027
[36]
NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins

K. D. Pruitt, T. Tatusova, D. R. Maglott

Nucleic Acids Research 2007 10.1093/nar/gkl842
[37]
Ramisetty "Horizontal gene transfer of chromosomal type II toxin–antitoxin systems of Escherichia coli" FEMS Microbiol Lett (2016) 10.1093/femsle/fnv238
[38]
Reams "Mechanisms of gene duplication and amplification" Cold Spring Harb Perspect Biol (2015) 10.1101/cshperspect.a016592
[39]
Robinson "A review of bacteria-animal lateral gene transfer may inform our understanding of diseases like cancer" PLoS Genet (2013) 10.1371/journal.pgen.1003877
[40]
Sela "Theory of prokaryotic genome evolution" Proc Natl Acad Sci U S A (2016) 10.1073/pnas.1614083113
[41]
Sheridan "Gene duplication drives genome expansion in a major lineage of Thaumarchaeota" Nat Commun (2020) 10.1038/s41467-020-19132-x
[42]
Snel "Genomes in flux: the evolution of archaeal and proteobacterial gene content" Genome Res (2002) 10.1101/gr.176501
[43]
Soppa "Polyploidy and community structure" Nature Microbiol (2017)
[44]
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

Alexandros Stamatakis

Bioinformatics 2014 10.1093/bioinformatics/btu033
[45]
Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

Gergely J. Szöllősi, Bastien Boussau, Sophie S. Abby et al.

Proceedings of the National Academy of Sciences 2012 10.1073/pnas.1202997109
[46]
Szöllősi "Genome-scale phylogenetic analysis finds extensive gene transfer among fungi" Philos Trans R Soc Lond B Biol Sci (2015) 10.1098/rstb.2014.0335
[47]
Treangen "Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes" PLoS Genet (2011) 10.1371/journal.pgen.1001284
[48]
Tria "Gene duplications trace mitochondria to the onset of eukaryote complexity" Genome Biol Evol (2021) 10.1093/gbe/evab055
[49]
Vos "Rates of lateral gene transfer in prokaryotes: high but why?" Trends Microbiol (2015) 10.1016/j.tim.2015.07.006
[50]
Wang "Phylogenomic analysis demonstrates a pattern of rare and long-lasting concerted evolution in prokaryotes" Commun Biol (2018) 10.1038/s42003-018-0014-x

Showing 50 of 54 references

Metrics
45
Citations
54
References
Details
Published
Oct 01, 2021
Vol/Issue
13(10)
License
View
Cite This Article
Fernando D K Tria, William F Martin (2021). Gene Duplications Are At Least 50 Times Less Frequent than Gene Transfers in Prokaryotic Genomes. Genome Biology and Evolution, 13(10). https://doi.org/10.1093/gbe/evab224