On the need for widespread horizontal gene transfers under genome size constraint.
BACKGROUND
While eukaryotes primarily evolve by duplication-divergence expansion (and reduction) of their own gene repertoire with only rare horizontal gene transfers, prokaryotes appear to evolve under both gene duplications and widespread horizontal gene transfers over long evolutionary time scales. But, the evolutionary origin of this striking difference in the importance of horizontal gene transfers remains by and large a mystery.


OBJECTIVE
We propose that the abundance of horizontal gene transfers in free-living prokaryotes is a simple but necessary consequence of two opposite effects: i) their apparent genome size constraint compared to typical eukaryote genomes and ii) their underlying genome expansion dynamics through gene duplication-divergence evolution, as demonstrated by the presence of many tandem and block repeated genes. In principle, this combination of genome size constraint and underlying duplication expansion should lead to a coalescent-like process with extensive turnover of functional genes. This would, however, imply the unlikely, systematic reinvention of functions from discarded genes within independent phylogenetic lineages. Instead, we propose that the long-term evolutionary adaptation of free-living prokaryotes must have resulted in the emergence of efficient non-phylogenetic pathways to circumvent gene loss.


CONCLUSIONS
This need for widespread horizontal gene transfers due to genome size constraint implies, in particular, that prokaryotes must remain under strong selection pressure in order to maintain the long-term evolutionary adaptation of their "mutualized" gene pool, beyond the inevitable turnover of individual prokaryote species. By contrast, the absence of genome size constraint for typical eukaryotes has presumably relaxed their need for widespread horizontal gene transfers and strong selection pressure. Yet, the resulting loss of genetic functions, due to weak selection pressure and inefficient gene recovery mechanisms, must have ultimately favored the emergence of more complex life styles and ecological integration of many eukaryotes.


METHODS
This article was reviewed by Pierre Pontarotti, Eugene V Koonin and Sergei Maslov.
Isambert
Hervé
H
Institut Curie, CNRS UMR168, 11 rue P, & M, Curie, 75005 Paris, France. herve.isambert@curie.fr
Stein
Richard R
RR
D022761:Gene Transfer, Horizontal / Q000235:genetics* / Q000502:physiology; D020745:Genome, Archaeal / Q000235:genetics*; D016680:Genome, Bacterial / Q000235:genetics*; D011387:Prokaryotic Cells / Q000378:metabolism*
Science. 2005 Aug 19;309(5738):1242-5
16109880
Anat Rec (Hoboken). 2007 Jun;290(6):514-22
17516441
PLoS Genet. 2009 Mar;5(3):e1000403
19266026
Nucleic Acids Res. 2002 Jul 1;30(13):2987-94
12087185
Annu Rev Microbiol. 2006;60:327-49
16824010
Evolution. 2006 Sep;60(9):1896-912
17089974
Nat Rev Genet. 2007 Oct;8(10):803-13
17878896
BMC Genomics. 2006 Feb 10;7:22
16472398
Trends Genet. 1998 Nov;14(11):442-4
9825671
Mol Biol Evol. 2002 Dec;19(12):2226-38
12446813
Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11647-52
16868079
Genome Res. 2006 May;16(5):636-43
16651664
Mol Biol Evol. 2005 Aug;22(8):1721-32
15901840
Trends Ecol Evol. 2004 Jun;19(6):278-80
16701270
Trends Genet. 2003 Sep;19(9):479-84
12957540
Biol Direct. 2008 Jul 09;3:29
18613974
Genes Dev. 2007 May 1;21(9):1010-24
17473168
Science. 2008 May 30;320(5880):1210-3
18511688
Nat Rev Microbiol. 2005 Sep;3(9):679-87
16138096
BMC Evol Biol. 2007 Feb 08;7 Suppl 1:S8
17288581
Mol Biosyst. 2009 Feb;5(2):170-9
19156263
Trends Microbiol. 2004 Apr;12(4):148-54
15116722
Nature. 2004 Sep 9;431(7005):152-5
15356622
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9743-8
19482938
Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):9863-8
18632555
Science. 2001 Jun 8;292(5523):1903-6
11358996
Proc Biol Sci. 1999 Aug 7;266(1428):1571-7
10467746
Mol Biol Evol. 2001 Mar;18(3):362-75
11230537
Evolution. 2008 Sep;62(9):2155-77
18616572
Science. 2006 Mar 24;311(5768):1730-3
16556833
BMC Syst Biol. 2007 Nov 13;1:49
17999763
Nat Rev Genet. 2008 Aug;9(8):605-18
18591983
Trends Ecol Evol. 2008 Nov;23(11):602-9
18814933
Genome Biol. 2006;7(10):118
17081279
Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5516-20
17372223
Nucleic Acids Res. 2008 Dec;36(21):6688-719
18948295
Science. 2006 Mar 3;311(5765):1283-7
16513982
Mol Biol Evol. 2007 Apr;24(4):969-81
17251179
Trends Genet. 2005 Jan;21(1):21-5
15680509
Proc Natl Acad Sci U S A. 2005 Nov 1;102(44):15971-6
16236728
BMC Genomics. 2008 May 20;9:235
18492275
Nature. 1999 May 27;399(6734):323-9
10360571