Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622.
The gene encoding the GroEL chaperonin is duplicated in nearly 30% of bacterial genomes; and although duplicated groEL genes have been comprehensively determined to have distinct physiological functions in different species, the mechanisms involved have not been characterized to date. Myxococcus xan...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2013-01-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC3578752?pdf=render |
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| author | Yan Wang Wen-yan Zhang Zheng Zhang Jian Li Zhi-feng Li Zai-gao Tan Tian-tian Zhang Zhi-hong Wu Hong Liu Yue-zhong Li |
| author_facet | Yan Wang Wen-yan Zhang Zheng Zhang Jian Li Zhi-feng Li Zai-gao Tan Tian-tian Zhang Zhi-hong Wu Hong Liu Yue-zhong Li |
| author_sort | Yan Wang |
| collection | DOAJ |
| description | The gene encoding the GroEL chaperonin is duplicated in nearly 30% of bacterial genomes; and although duplicated groEL genes have been comprehensively determined to have distinct physiological functions in different species, the mechanisms involved have not been characterized to date. Myxococcus xanthus DK1622 has two copies of the groEL gene, each of which can be deleted without affecting cell viability; however, the deletion of either gene does result in distinct defects in the cellular heat-shock response, predation, and development. In this study, we show that, from the expression levels of different groELs, the distinct functions of groEL1 and groEL2 in predation and development are probably the result of the substrate selectivity of the paralogous GroEL chaperonins, whereas the lethal effect of heat shock due to the deletion of groEL1 is caused by a decrease in the total groEL expression level. Following a bioinformatics analysis of the composition characteristics of GroELs from different bacteria, we performed region-swapping assays in M. xanthus, demonstrating that the differences in the apical and the C-terminal equatorial regions determine the substrate specificity of the two GroELs. Site-directed mutagenesis experiments indicated that the GGM repeat sequence at the C-terminus of GroEL1 plays an important role in functional divergence. Divergent functions of duplicated GroELs, which have similar patterns of variation in different bacterial species, have thus evolved mainly via alteration of the apical and the C-terminal equatorial regions. We identified the specific substrates of strain DK1622's GroEL1 and GroEL2 using immunoprecipitation and mass spectrometry techniques. Although 68 proteins bound to both GroEL1 and GroEL2, 83 and 46 proteins bound exclusively to GroEL1 or GroEL2, respectively. The GroEL-specific substrates exhibited distinct molecular sizes and secondary structures, providing an encouraging indication for GroEL evolution for functional divergence. |
| first_indexed | 2024-12-19T21:45:28Z |
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| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-19T21:45:28Z |
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| series | PLoS Genetics |
| spelling | doaj.art-d5dc5dd74d9b4d1abd9e88e0bbc861772022-12-21T20:04:33ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042013-01-0192e100330610.1371/journal.pgen.1003306Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622.Yan WangWen-yan ZhangZheng ZhangJian LiZhi-feng LiZai-gao TanTian-tian ZhangZhi-hong WuHong LiuYue-zhong LiThe gene encoding the GroEL chaperonin is duplicated in nearly 30% of bacterial genomes; and although duplicated groEL genes have been comprehensively determined to have distinct physiological functions in different species, the mechanisms involved have not been characterized to date. Myxococcus xanthus DK1622 has two copies of the groEL gene, each of which can be deleted without affecting cell viability; however, the deletion of either gene does result in distinct defects in the cellular heat-shock response, predation, and development. In this study, we show that, from the expression levels of different groELs, the distinct functions of groEL1 and groEL2 in predation and development are probably the result of the substrate selectivity of the paralogous GroEL chaperonins, whereas the lethal effect of heat shock due to the deletion of groEL1 is caused by a decrease in the total groEL expression level. Following a bioinformatics analysis of the composition characteristics of GroELs from different bacteria, we performed region-swapping assays in M. xanthus, demonstrating that the differences in the apical and the C-terminal equatorial regions determine the substrate specificity of the two GroELs. Site-directed mutagenesis experiments indicated that the GGM repeat sequence at the C-terminus of GroEL1 plays an important role in functional divergence. Divergent functions of duplicated GroELs, which have similar patterns of variation in different bacterial species, have thus evolved mainly via alteration of the apical and the C-terminal equatorial regions. We identified the specific substrates of strain DK1622's GroEL1 and GroEL2 using immunoprecipitation and mass spectrometry techniques. Although 68 proteins bound to both GroEL1 and GroEL2, 83 and 46 proteins bound exclusively to GroEL1 or GroEL2, respectively. The GroEL-specific substrates exhibited distinct molecular sizes and secondary structures, providing an encouraging indication for GroEL evolution for functional divergence.http://europepmc.org/articles/PMC3578752?pdf=render |
| spellingShingle | Yan Wang Wen-yan Zhang Zheng Zhang Jian Li Zhi-feng Li Zai-gao Tan Tian-tian Zhang Zhi-hong Wu Hong Liu Yue-zhong Li Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622. PLoS Genetics |
| title | Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622. |
| title_full | Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622. |
| title_fullStr | Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622. |
| title_full_unstemmed | Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622. |
| title_short | Mechanisms involved in the functional divergence of duplicated GroEL chaperonins in Myxococcus xanthus DK1622. |
| title_sort | mechanisms involved in the functional divergence of duplicated groel chaperonins in myxococcus xanthus dk1622 |
| url | http://europepmc.org/articles/PMC3578752?pdf=render |
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