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Evolution and dynamics of megaplasmids with genome sizes larger than 100 kb in the Bacillus cereus group.

Zheng J, Peng D, Ruan L, Sun M - BMC Evol. Biol. (2013)

Bottom Line: Therefore, we speculated that these megaplasmids are the results of fusion of smaller plasmids.Megaplasmids of B. cereus group are fusion of smaller plasmids, and the fusion of plasmids likely occurs frequently in the B. cereus group and in other bacterial taxa.Plasmid fusion may be one of the major mechanisms for formation of novel megaplasmids in the evolution of bacteria.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China. m98sun@mail.hzau.edu.cn.

ABSTRACT

Background: Plasmids play a crucial role in the evolution of bacterial genomes by mediating horizontal gene transfer. However, the origin and evolution of most plasmids remains unclear, especially for megaplasmids. Strains of the Bacillus cereus group contain up to 13 plasmids with genome sizes ranging from 2 kb to 600 kb, and thus can be used to study plasmid dynamics and evolution.

Results: This work studied the origin and evolution of 31 B. cereus group megaplasmids (>100 kb) focusing on the most conserved regions on plasmids, minireplicons. Sixty-five putative minireplicons were identified and classified to six types on the basis of proteins that are essential for replication. Twenty-nine of the 31 megaplasmids contained two or more minireplicons. Phylogenetic analysis of the protein sequences showed that different minireplicons on the same megaplasmid have different evolutionary histories. Therefore, we speculated that these megaplasmids are the results of fusion of smaller plasmids. All plasmids of a bacterial strain must be compatible. In megaplasmids of the B. cereus group, individual minireplicons of different megaplasmids in the same strain belong to different types or subtypes. Thus, the subtypes of each minireplicon they contain may determine the incompatibilities of megaplasmids. A broader analysis of all 1285 bacterial plasmids with putative known minireplicons whose complete genome sequences were available from GenBank revealed that 34% (443 plasmids) of the plasmids have two or more minireplicons. This indicates that plasmid fusion events are general among bacterial plasmids.

Conclusions: Megaplasmids of B. cereus group are fusion of smaller plasmids, and the fusion of plasmids likely occurs frequently in the B. cereus group and in other bacterial taxa. Plasmid fusion may be one of the major mechanisms for formation of novel megaplasmids in the evolution of bacteria.

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Comparison of the genomes of pBMB137, pBMB65 and pBMB95. From the inside: pBMB137, pBMB65 and pBMB95.
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Figure 4: Comparison of the genomes of pBMB137, pBMB65 and pBMB95. From the inside: pBMB137, pBMB65 and pBMB95.

Mentions: As mentioned above, two or more different putative minireplicons generally occur in the same megaplasmids in B. cereus group. This may indicate that these megaplasmids have resulted from the integration of two or more smaller plasmids. Minireplicons of the four tubZ/tubR subtypes and pXO1-14/pXO1-16 were not found in plasmids with only one minireplicon. Of the megaplasmids whose genome sequences were available, we observed that minireplicon pXO1-14/pXO1-16 frequently coexists with one of the four tubZ/tubR subtypes. These megaplasmids may share similar origins and are probably the result of a fusion between an ancestral pXO1-14/pXO1-16-like plasmid and an ancestral tubZ/tubR plasmid early in evolutionary history. For other megaplasmids, such as those containing ori44, ori60 and repA_N, the minireplicons they contained were also found on smaller plasmids which usually have only one minireplicon. These minireplicons thus exist as sole replicon for small plasmids and as one of several minireplicons on megaplasmids. Direct evidence for this situation is provided by comparing pBMB137 of B. thuringiensis YBT-1520 to pBMB65 and pBMB95 of B. thuringiensis HD1. Plasmid pBMB137 has a genome size of 137,573 bp and contains the minireplicons ori44 and ori60. B. thuringiensis HD1 harbours the 65 kb plasmid pBMB65 with minireplicon ori44, and the 95 kb plasmid pBMB95, with minireplicon ori60. The genome sequence of pBMB137 can be divided into two fragments, one of which is virtually identical to pBMB65, and the other shows a high level of similarity to pBMB95 (Figure 4). Unlike the ancestral event that formed the pXO1-like plasmids, this fusion is a recent event as the separate and smaller plasmids are maintained by some strains while others maintain with the integrated megaplasmid.


Evolution and dynamics of megaplasmids with genome sizes larger than 100 kb in the Bacillus cereus group.

Zheng J, Peng D, Ruan L, Sun M - BMC Evol. Biol. (2013)

Comparison of the genomes of pBMB137, pBMB65 and pBMB95. From the inside: pBMB137, pBMB65 and pBMB95.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4219350&req=5

Figure 4: Comparison of the genomes of pBMB137, pBMB65 and pBMB95. From the inside: pBMB137, pBMB65 and pBMB95.
Mentions: As mentioned above, two or more different putative minireplicons generally occur in the same megaplasmids in B. cereus group. This may indicate that these megaplasmids have resulted from the integration of two or more smaller plasmids. Minireplicons of the four tubZ/tubR subtypes and pXO1-14/pXO1-16 were not found in plasmids with only one minireplicon. Of the megaplasmids whose genome sequences were available, we observed that minireplicon pXO1-14/pXO1-16 frequently coexists with one of the four tubZ/tubR subtypes. These megaplasmids may share similar origins and are probably the result of a fusion between an ancestral pXO1-14/pXO1-16-like plasmid and an ancestral tubZ/tubR plasmid early in evolutionary history. For other megaplasmids, such as those containing ori44, ori60 and repA_N, the minireplicons they contained were also found on smaller plasmids which usually have only one minireplicon. These minireplicons thus exist as sole replicon for small plasmids and as one of several minireplicons on megaplasmids. Direct evidence for this situation is provided by comparing pBMB137 of B. thuringiensis YBT-1520 to pBMB65 and pBMB95 of B. thuringiensis HD1. Plasmid pBMB137 has a genome size of 137,573 bp and contains the minireplicons ori44 and ori60. B. thuringiensis HD1 harbours the 65 kb plasmid pBMB65 with minireplicon ori44, and the 95 kb plasmid pBMB95, with minireplicon ori60. The genome sequence of pBMB137 can be divided into two fragments, one of which is virtually identical to pBMB65, and the other shows a high level of similarity to pBMB95 (Figure 4). Unlike the ancestral event that formed the pXO1-like plasmids, this fusion is a recent event as the separate and smaller plasmids are maintained by some strains while others maintain with the integrated megaplasmid.

Bottom Line: Therefore, we speculated that these megaplasmids are the results of fusion of smaller plasmids.Megaplasmids of B. cereus group are fusion of smaller plasmids, and the fusion of plasmids likely occurs frequently in the B. cereus group and in other bacterial taxa.Plasmid fusion may be one of the major mechanisms for formation of novel megaplasmids in the evolution of bacteria.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China. m98sun@mail.hzau.edu.cn.

ABSTRACT

Background: Plasmids play a crucial role in the evolution of bacterial genomes by mediating horizontal gene transfer. However, the origin and evolution of most plasmids remains unclear, especially for megaplasmids. Strains of the Bacillus cereus group contain up to 13 plasmids with genome sizes ranging from 2 kb to 600 kb, and thus can be used to study plasmid dynamics and evolution.

Results: This work studied the origin and evolution of 31 B. cereus group megaplasmids (>100 kb) focusing on the most conserved regions on plasmids, minireplicons. Sixty-five putative minireplicons were identified and classified to six types on the basis of proteins that are essential for replication. Twenty-nine of the 31 megaplasmids contained two or more minireplicons. Phylogenetic analysis of the protein sequences showed that different minireplicons on the same megaplasmid have different evolutionary histories. Therefore, we speculated that these megaplasmids are the results of fusion of smaller plasmids. All plasmids of a bacterial strain must be compatible. In megaplasmids of the B. cereus group, individual minireplicons of different megaplasmids in the same strain belong to different types or subtypes. Thus, the subtypes of each minireplicon they contain may determine the incompatibilities of megaplasmids. A broader analysis of all 1285 bacterial plasmids with putative known minireplicons whose complete genome sequences were available from GenBank revealed that 34% (443 plasmids) of the plasmids have two or more minireplicons. This indicates that plasmid fusion events are general among bacterial plasmids.

Conclusions: Megaplasmids of B. cereus group are fusion of smaller plasmids, and the fusion of plasmids likely occurs frequently in the B. cereus group and in other bacterial taxa. Plasmid fusion may be one of the major mechanisms for formation of novel megaplasmids in the evolution of bacteria.

Show MeSH
Related in: MedlinePlus