Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2

BAX inhibitor 1 (BI-1) is an evolutionarily conserved transmembrane protein first identified in a screening process for human proteins that suppress BAX-induced apoptosis in yeast cells. Eukaryotic BI-1 is a cytoprotective protein that suppresses cell death induced by multiple stimuli in eukaryotes....

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Main Authors: Guangdong Zhang, Fangli Zhong, Lei Chen, Peipei Qin, Junmei Li, Feijie Zhi, Lulu Tian, Dong Zhou, Pengfei Lin, Huatao Chen, Keqiong Tang, Wei Liu, Yaping Jin, Aihua Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.632095/full
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language English
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author Guangdong Zhang
Guangdong Zhang
Fangli Zhong
Fangli Zhong
Lei Chen
Lei Chen
Peipei Qin
Peipei Qin
Junmei Li
Junmei Li
Feijie Zhi
Feijie Zhi
Lulu Tian
Lulu Tian
Dong Zhou
Dong Zhou
Pengfei Lin
Pengfei Lin
Huatao Chen
Huatao Chen
Keqiong Tang
Keqiong Tang
Wei Liu
Wei Liu
Yaping Jin
Yaping Jin
Aihua Wang
Aihua Wang
spellingShingle Guangdong Zhang
Guangdong Zhang
Fangli Zhong
Fangli Zhong
Lei Chen
Lei Chen
Peipei Qin
Peipei Qin
Junmei Li
Junmei Li
Feijie Zhi
Feijie Zhi
Lulu Tian
Lulu Tian
Dong Zhou
Dong Zhou
Pengfei Lin
Pengfei Lin
Huatao Chen
Huatao Chen
Keqiong Tang
Keqiong Tang
Wei Liu
Wei Liu
Yaping Jin
Yaping Jin
Aihua Wang
Aihua Wang
Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2
Frontiers in Microbiology
Brucella suis S2
BAX inhibitor 1 (BI-1)
cell viability
cell division
membrane homeostasis
stress resistance
author_facet Guangdong Zhang
Guangdong Zhang
Fangli Zhong
Fangli Zhong
Lei Chen
Lei Chen
Peipei Qin
Peipei Qin
Junmei Li
Junmei Li
Feijie Zhi
Feijie Zhi
Lulu Tian
Lulu Tian
Dong Zhou
Dong Zhou
Pengfei Lin
Pengfei Lin
Huatao Chen
Huatao Chen
Keqiong Tang
Keqiong Tang
Wei Liu
Wei Liu
Yaping Jin
Yaping Jin
Aihua Wang
Aihua Wang
author_sort Guangdong Zhang
title Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2
title_short Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2
title_full Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2
title_fullStr Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2
title_full_unstemmed Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2
title_sort integrated proteomic and transcriptomic analyses reveal the roles of brucella homolog of bax inhibitor 1 in cell division and membrane homeostasis of brucella suis s2
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-01-01
description BAX inhibitor 1 (BI-1) is an evolutionarily conserved transmembrane protein first identified in a screening process for human proteins that suppress BAX-induced apoptosis in yeast cells. Eukaryotic BI-1 is a cytoprotective protein that suppresses cell death induced by multiple stimuli in eukaryotes. Brucella, the causative agent of brucellosis that threatens public health and animal husbandry, contains a conserved gene that encodes BI-1-like protein. To explore the role of the Brucella homolog of BI-1, BrBI, in Brucella suis S2, we constructed the brbI deletion mutant strain and its complemented strain. brbI deletion altered the membrane properties of Brucella suis S2 and decreased its resistance to acidic pH, H2O2, polymyxin B, and lincomycin. Additionally, deleting brbI led to defective growth, cell division, and viability in Brucella suis S2. We then revealed the effect of brbI deletion on the physiological characteristics of Brucella suis S2 via integrated transcriptomic and proteomic analyses. The integrated analysis showed that brbI deletion significantly affected the expression of multiple genes at the mRNA and/or protein levels. Specifically, the affected divisome proteins, FtsB, FtsI, FtsL, and FtsQ, may be the molecular basis of the impaired cell division of the brbI mutant strain, and the extensively affected membrane proteins and transporter-associated proteins were consistent with the phenotype of the membrane properties’ alterations of the brbI mutant strain. In conclusion, our results revealed that BrBI is a bacterial cytoprotective protein involved in membrane homeostasis, cell division, and stress resistance in Brucella suis S2.
topic Brucella suis S2
BAX inhibitor 1 (BI-1)
cell viability
cell division
membrane homeostasis
stress resistance
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.632095/full
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spelling doaj-5bc4c70cc5024cda8789fa197f0529f02021-01-28T09:04:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-01-011210.3389/fmicb.2021.632095632095Integrated Proteomic and Transcriptomic Analyses Reveal the Roles of Brucella Homolog of BAX Inhibitor 1 in Cell Division and Membrane Homeostasis of Brucella suis S2Guangdong Zhang0Guangdong Zhang1Fangli Zhong2Fangli Zhong3Lei Chen4Lei Chen5Peipei Qin6Peipei Qin7Junmei Li8Junmei Li9Feijie Zhi10Feijie Zhi11Lulu Tian12Lulu Tian13Dong Zhou14Dong Zhou15Pengfei Lin16Pengfei Lin17Huatao Chen18Huatao Chen19Keqiong Tang20Keqiong Tang21Wei Liu22Wei Liu23Yaping Jin24Yaping Jin25Aihua Wang26Aihua Wang27College of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, ChinaKey Laboratory of Animal Biotechnology, Ministry of Agriculture, Northwest A&F University, Yangling, ChinaBAX inhibitor 1 (BI-1) is an evolutionarily conserved transmembrane protein first identified in a screening process for human proteins that suppress BAX-induced apoptosis in yeast cells. Eukaryotic BI-1 is a cytoprotective protein that suppresses cell death induced by multiple stimuli in eukaryotes. Brucella, the causative agent of brucellosis that threatens public health and animal husbandry, contains a conserved gene that encodes BI-1-like protein. To explore the role of the Brucella homolog of BI-1, BrBI, in Brucella suis S2, we constructed the brbI deletion mutant strain and its complemented strain. brbI deletion altered the membrane properties of Brucella suis S2 and decreased its resistance to acidic pH, H2O2, polymyxin B, and lincomycin. Additionally, deleting brbI led to defective growth, cell division, and viability in Brucella suis S2. We then revealed the effect of brbI deletion on the physiological characteristics of Brucella suis S2 via integrated transcriptomic and proteomic analyses. The integrated analysis showed that brbI deletion significantly affected the expression of multiple genes at the mRNA and/or protein levels. Specifically, the affected divisome proteins, FtsB, FtsI, FtsL, and FtsQ, may be the molecular basis of the impaired cell division of the brbI mutant strain, and the extensively affected membrane proteins and transporter-associated proteins were consistent with the phenotype of the membrane properties’ alterations of the brbI mutant strain. In conclusion, our results revealed that BrBI is a bacterial cytoprotective protein involved in membrane homeostasis, cell division, and stress resistance in Brucella suis S2.https://www.frontiersin.org/articles/10.3389/fmicb.2021.632095/fullBrucella suis S2BAX inhibitor 1 (BI-1)cell viabilitycell divisionmembrane homeostasisstress resistance