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BMC Genomics. 2015 Dec 21;16:1084. doi: 10.1186/s12864-015-2288-4.

Lifespan of restriction-modification systems critically affects avoidance of their recognition sites in host genomes.

Rusinov I1, Ershova A2,3,4, Karyagina A5,6,7, Spirin S8,9,10, Alexeevski A11,12,13.

Author information

1
Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, 119992, Russia. isrusinov@gmail.com.
2
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119992, Russia. asershova@gmail.com.
3
Gamaleya Center of Epidemiology and Microbiology, Moscow, 123098, Russia. asershova@gmail.com.
4
Institute of Agricultural Biotechnology, the Russian Academy of Sciences, Moscow, 127550, Russia. asershova@gmail.com.
5
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119992, Russia. akaryagina@gmail.com.
6
Gamaleya Center of Epidemiology and Microbiology, Moscow, 123098, Russia. akaryagina@gmail.com.
7
Institute of Agricultural Biotechnology, the Russian Academy of Sciences, Moscow, 127550, Russia. akaryagina@gmail.com.
8
Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, 119992, Russia. sas@belozersky.msu.ru.
9
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119992, Russia. sas@belozersky.msu.ru.
10
Scientific Research Institute for System Studies, the Russian Academy of Science (NIISI RAS), Moscow, 117281, Russia. sas@belozersky.msu.ru.
11
Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, 119992, Russia. aba@belozersky.msu.ru.
12
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow, 119992, Russia. aba@belozersky.msu.ru.
13
Scientific Research Institute for System Studies, the Russian Academy of Science (NIISI RAS), Moscow, 117281, Russia. aba@belozersky.msu.ru.

Abstract

BACKGROUND:

Avoidance of palindromic recognition sites of Type II restriction-modification (R-M) systems was shown for many R-M systems in dozens of prokaryotic genomes. However the phenomenon has not been investigated systematically for all presently available genomes and annotated R-M systems. We have studied all known recognition sites in thousands of prokaryotic genomes and found factors that influence their avoidance.

RESULTS:

Only Type II R-M systems consisting of independently acting endonuclease and methyltransferase (called 'orthodox' here) cause avoidance of their sites, both palindromic and asymmetric, in corresponding prokaryotic genomes; the avoidance takes place for ~ 50 % of 1774 studied cases. It is known that prokaryotes can acquire and lose R-M systems. Thus it is possible to talk about the lifespan of an R-M system in a genome. We have shown that the recognition site avoidance correlates with the lifespan of R-M systems. The sites of orthodox R-M systems that are encoded in host genomes for a long time are avoided more often (up to 100 % in certain cohorts) than the sites of recently acquired ones. We also found cases of site avoidance in absence of the corresponding R-M systems in the genome. An analysis of closely related bacteria shows that such avoidance can be a trace of lost R-M systems. Sites of Type I, IIС/G, IIM, III, and IV R-M systems are not avoided in vast majority of cases.

CONCLUSIONS:

The avoidance of orthodox Type II R-M system recognition sites in prokaryotic genomes is a widespread phenomenon. Presence of an R-M system without an underrepresentation of its site may indicate that the R-M system was acquired recently. At the same time, a significant underrepresentation of a site may be a sign of presence of the corresponding R-M system in this organism or in its ancestors for a long time. The drastic difference between site avoidance for orthodox Type II R-M systems and R-M systems of other types can be explained by a higher rate of specificity changes or a less self-toxicity of the latter.

PMID:
26689194
PMCID:
PMC4687349
DOI:
10.1186/s12864-015-2288-4
[Indexed for MEDLINE]
Free PMC Article

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