Gluconate 5-dehydrogenase (Ga5DH) participates in <i>Streptococcus suis</i> cell division

doi:10.1007/s13238-014-0074-8

Protein Cell

2014, Vol. 5

Issue (10) : 761-769 https://doi.org/10.1007/s13238-014-0074-8

RESEARCH ARTICLE

Gluconate 5-dehydrogenase (Ga5DH) participates in Streptococcus suis cell division

Zhongyu Shi^1,²,Chunling Xuan^1,²,Huiming Han¹,Xia Cheng^1,³,Jundong Wang³,Youjun Feng⁴,Swaminath Srinivas⁵,Guangwen Lu¹,George F. Gao^1,^2,^6,^7,^*(

)

1. CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
2. University of Chinese Academy of Sciences, Beijing 100049, China
3. College of Animal Science and Technology, Shanxi Agricultural University, Taigu 030801, China
4. Department of Microbiology, University of Illinois, Urbana, IL 61801, USA
5. Department of Biochemistry, University of Illinois, Urbana, IL 61801, USA
6. Laboratory of Protein Engineering and Vaccines, Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin 300308, China
7. Research Network of Immunity and Health (RNIH), Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China

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Abstract

Bacterial cell division is strictly regulated in the formation of equal daughter cells. This process is governed by a series of spatial and temporal regulators, and several new factors of interest to the field have recently been identified. Here, we report the requirement of gluconate 5-dehydrogenase (Ga5DH) in cell division of the zoonotic pathogen Streptococcus suis. Ga5DH catalyzes the reversible reduction of 5-ketogluconate to D-gluconate and was localized to the site of cell division. The deletion of Ga5DH in S. suis resulted in a plump morphology with aberrant septa joining the progeny. A significant increase was also observed in cell length. These defects were determined to be the consequence of Ga5DH deprivation in S. suis causing FtsZ delocalization. In addition, the interaction of FtsZ with Ga5DH in vitro was confirmed by protein interaction assays. These results indicate that Ga5DH may function to prevent the formation of ectopic Z rings during S. suis cell division.

Keywords Streptococcus suis Ga5DH cell shape cell division FtsZ localization

Corresponding Author(s): George F. Gao

Issue Date: 24 October 2014

Cite this article:

Zhongyu Shi,Chunling Xuan,Huiming Han, et al. Gluconate 5-dehydrogenase (Ga5DH) participates in Streptococcus suis cell division[J]. Protein Cell, 2014, 5(10): 761-769.

URL:

https://academic.hep.com.cn/pac/EN/10.1007/s13238-014-0074-8
https://academic.hep.com.cn/pac/EN/Y2014/V5/I10/761

1	Addinall SG, Lutkenhaus J (1996) FtsZ-spirals and-arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol Microbiol22: 231-237 https://doi.org/10.1046/j.1365-2958.1996.00100.x
2	Albarracin Orio AG, Pinas GE, Cortes PR, Cian MB, Echenique J (2011) Compensatory evolution of pbp mutations restores the fitness cost imposed by β-lactam resistance in Streptococcus pneumoniae. PLoS Pathog7: e1002000 https://doi.org/10.1371/journal.ppat.1002000
3	Bi EF, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature354: 161-164 https://doi.org/10.1038/354161a0
4	Dziedzic R, Kiran M, Plocinski P, Ziolkiewicz M, Brzostek A, Moomey M, Vadrevu IS, Dziadek J, Madiraju M, Rajagopalan M (2010) Mycobacterium tuberculosis ClpX interacts with FtsZ and interferes with FtsZ assembly. PloS One5: e11058 https://doi.org/10.1371/journal.pone.0011058
5	Elbaz M, Ben-Yehuda S (2010) The metabolic enzyme ManA reveals a link between cell wall integrity and chromosome morphology. PLoS Genet6: e1001119 https://doi.org/10.1371/journal.pgen.1001119
6	Feng Y, Zheng F, Pan X, Sun W, Wang C, Dong Y, Ju A, Ge J, Liu D, Liu C (2007) Existence and characterization of allelic variants of Sao, a newly identified surface protein from Streptococcus suis. FEMS Microbiol Lett275: 80-88 https://doi.org/10.1111/j.1574-6968.2007.00859.x
7	Feng Y, Li M, Zhang H, Zheng B, Han H, Wang C, Yan J, Tang J, Gao GF (2008) Functional definition and global regulation of Zur, a zinc uptake regulator in a Streptococcus suis serotype 2 strain causing streptococcal toxic shock syndrome. J Bacteriol190: 7567-7578 https://doi.org/10.1128/JB.01532-07
8	Feng Y, Shi X, Zhang H, Zhang S, Ma Y, Zheng B, Han H, Lan Q, Tang J, Cheng J (2009) Recurrence of human Streptococcus suis infections in 2007: three cases of meningitis and implications that heterogeneous S. suis 2 circulates in China. Zoonoses Public Health56: 506-514 https://doi.org/10.1111/j.1863-2378.2008.01225.x
9	Feng Y, Zhang H, Ma Y, Gao GF (2010) Uncovering newly emerging variants of Streptococcus suis, an important zoonotic agent. Trends Microbiol18: 124-131 https://doi.org/10.1016/j.tim.2009.12.003
10	Fleurie A, Cluzel C, Guiral S, Freton C, Galisson F, Zanella-Cleon I, Di Guilmi AM, Grangeasse C (2012) Mutational dissection of the S/T-kinase StkP reveals crucial roles in cell division of Streptococcus pneumoniae.Mol Microbiol83: 746-758 https://doi.org/10.1111/j.1365-2958.2011.07962.x
11	Foulquier E, Pompeo F, Bernadac A, Espinosa L, Galinier A (2011) The YvcK protein is required for morphogenesis via localization of PBP1 under gluconeogenic growth conditions in Bacillus subtilis. Mol Microbiol80: 309-318 https://doi.org/10.1111/j.1365-2958.2011.07587.x
12	Kay R, Cheng AF, Tse CY (1995) Streptococcus suis infection in Hong Kong. QJM88: 39-47
13	Li M, Wang C, Feng Y, Pan X, Cheng G, Wang J, Ge J, Zheng F, Cao M, Dong Y (2008) SalK/SalR, a two-component signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2. PLoS One3: e2080 https://doi.org/10.1371/journal.pone.0002080
14	Li M, Shen X, Yan J, Han H, Zheng B, Liu D, Cheng H, Zhao Y, Rao X, Wang C (2011) GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2. Mol Microbiol79: 1670-1683 https://doi.org/10.1111/j.1365-2958.2011.07553.x
15	Lu Q, Lu H, Qi J, Lu G, Gao GF (2012) An octamer of enolase from Streptococcus suis. Protein Cell3: 769-780 https://doi.org/10.1007/s13238-012-2040-7
16	Macrina FL, Tobian JA, Jones KR, Evans RP, Clewell DB (1982) A cloning vector able to replicate in Escherichia coli and Streptococcus sanguis. Gene19: 345-353 https://doi.org/10.1016/0378-1119(82)90025-7
17	Mazokopakis EE, Kofteridis DP, Papadakis JA, Gikas AH, Samonis GJ (2005) First case report of Streptococcus suis septicaemia and meningitis from Greece. Eur J Neurol12: 487-489 https://doi.org/10.1111/j.1468-1331.2005.00998.x
18	Nghia HD, Hoa NT, le Linh D, Campbell J, Diep TS, Chau NV, Mai NT, Hien TT, Spratt B, Farrar J (2008) Human case of Streptococcus suis serotype 16 infection. Emerg Infect Dis14: 155-157 https://doi.org/10.3201/eid1401.070534
19	Pichoff S, Lutkenhaus J (2002) Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J21: 685-693 https://doi.org/10.1093/emboj/21.4.685
20	Sweeney NJ, Laux DC, Cohen PS (1996) Escherichia coli F-18 and E. coli K-12 eda mutants do not colonize the streptomycin-treated mouse large intestine. Infect Immun64: 3504-3511
21	Tang J, Wang C, Feng Y, Yang W, Song H, Chen Z, Yu H, Pan X, Zhou X, Wang H (2006) Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med3: e151 https://doi.org/10.1371/journal.pmed.0030151
22	Weart RB, Lee AH, Chien AC, Haeusser DP, Hill NS, Levin PA (2007) A metabolic sensor governing cell size in bacteria. Cell130: 335-347 https://doi.org/10.1016/j.cell.2007.05.043
23	Zapun A, Vernet T, Pinho MG (2008) The different shapes of cocci. FEMS Microbiol Rev32: 345-360 https://doi.org/10.1111/j.1574-6976.2007.00098.x
24	Zhang Q, Peng H, Gao F, Liu Y, Cheng H, Thompson J, Gao GF (2009) Structural insight into the catalytic mechanism of gluconate 5-dehydrogenase from Streptococcus suis: crystal structures of the substrate-free and quaternary complex enzymes. Protein Sci18: 294-303 https://doi.org/10.1002/pro.32

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