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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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Phylogenetic trees constructed using the ML method based on TubZ (A) protein sequences and tubR DNA sequences (B for rep466-like, C for rep228-like and D for orf156/orf157-like) from plasmids of the B. cereus group species. The four subtrees in (A) represent the four subtypes of TubZ/TubR minireplicons. Plasmids from the same strain are marked in the same color. The number at each branch point represents the percentage of bootstrap support calculated from 1,000 replicates, and only those values higher than 50 are shown.
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Figure 1: Phylogenetic trees constructed using the ML method based on TubZ (A) protein sequences and tubR DNA sequences (B for rep466-like, C for rep228-like and D for orf156/orf157-like) from plasmids of the B. cereus group species. The four subtrees in (A) represent the four subtypes of TubZ/TubR minireplicons. Plasmids from the same strain are marked in the same color. The number at each branch point represents the percentage of bootstrap support calculated from 1,000 replicates, and only those values higher than 50 are shown.

Mentions: The minireplicon tubZ/tubR is distributed widely among the megaplasmids and is found in 26 of the 31 megaplasmids (Table 1). A phylogenetic tree was constructed based on the 26 TubZ protein sequences (Figure 1A). Four different clades were formed and were supported by high bootstrap values (100%). Coincidentally, four of the TubZ proteins for which a function in replication was validated, RepX in plasmid pXO1 [19], ORF156 in plasmid pBtoxis [21], Rep228-TubZ in plasmid pBMB228 and Rep466-TubZ in plasmid pBMB28 are located in the four different clades, respectively. The replication function of Rep228-TubZ and Rep446-TubZ were validated in this study (see Additional file 2). We divided all 26 tubZ/tubR minireplicons into four subtypes: repX-like, orf156/orf157-like, rep228-like and rep466-like. Among the four subtypes, only minireplicon repX-like encodes an orphan TubZ protein, while the other three encode not only TubZ proteins, but also TubR proteins. TubR proteins from different subtypes show no similarity to each other. However, when the gene sequences of TubR within each subtype were inspected, we found that the topologies of the phylogenetic trees showed similarities to those of the corresponding TubZ trees (Figures 1B, C and D), respectively. The DNA sequences of the origins of replication are rich in A + T and usually contain direct or invert repeats were additionally examined. The four minireplicon subtypes of tubZ/tubR have four different secondary structures of them, with different direct or inverted repeats (Additional file 3: Figure S4). We therefore suggest that for each subtype of tubZ/tubR minireplicon, their TubZ, TubR proteins and the corresponding origin of replication underwent a concerted evolution.


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)

Phylogenetic trees constructed using the ML method based on TubZ (A) protein sequences and tubR DNA sequences (B for rep466-like, C for rep228-like and D for orf156/orf157-like) from plasmids of the B. cereus group species. The four subtrees in (A) represent the four subtypes of TubZ/TubR minireplicons. Plasmids from the same strain are marked in the same color. The number at each branch point represents the percentage of bootstrap support calculated from 1,000 replicates, and only those values higher than 50 are shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Phylogenetic trees constructed using the ML method based on TubZ (A) protein sequences and tubR DNA sequences (B for rep466-like, C for rep228-like and D for orf156/orf157-like) from plasmids of the B. cereus group species. The four subtrees in (A) represent the four subtypes of TubZ/TubR minireplicons. Plasmids from the same strain are marked in the same color. The number at each branch point represents the percentage of bootstrap support calculated from 1,000 replicates, and only those values higher than 50 are shown.
Mentions: The minireplicon tubZ/tubR is distributed widely among the megaplasmids and is found in 26 of the 31 megaplasmids (Table 1). A phylogenetic tree was constructed based on the 26 TubZ protein sequences (Figure 1A). Four different clades were formed and were supported by high bootstrap values (100%). Coincidentally, four of the TubZ proteins for which a function in replication was validated, RepX in plasmid pXO1 [19], ORF156 in plasmid pBtoxis [21], Rep228-TubZ in plasmid pBMB228 and Rep466-TubZ in plasmid pBMB28 are located in the four different clades, respectively. The replication function of Rep228-TubZ and Rep446-TubZ were validated in this study (see Additional file 2). We divided all 26 tubZ/tubR minireplicons into four subtypes: repX-like, orf156/orf157-like, rep228-like and rep466-like. Among the four subtypes, only minireplicon repX-like encodes an orphan TubZ protein, while the other three encode not only TubZ proteins, but also TubR proteins. TubR proteins from different subtypes show no similarity to each other. However, when the gene sequences of TubR within each subtype were inspected, we found that the topologies of the phylogenetic trees showed similarities to those of the corresponding TubZ trees (Figures 1B, C and D), respectively. The DNA sequences of the origins of replication are rich in A + T and usually contain direct or invert repeats were additionally examined. The four minireplicon subtypes of tubZ/tubR have four different secondary structures of them, with different direct or inverted repeats (Additional file 3: Figure S4). We therefore suggest that for each subtype of tubZ/tubR minireplicon, their TubZ, TubR proteins and the corresponding origin of replication underwent a concerted evolution.

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