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Interactions between Clostridium difficile and Bacillus subtil
Interactions between Clostridium difficile and Bacillus subtilis Min systems Jana Makroczyová, Ján Jamroškovič, Naďa Pavlendová, Eva Krascsenitsová, Imrich Barák Institute of Molecular Biology, Slovak Academy of Sciences, Dúbravská cesta 21, 845 51 Bratislava, Slovakia jana.makroczyova@savba.sk
Introduction Gram-positive Bacillus subtilis and Gram-negative
Introduction Gram-positive Bacillus subtilis and Gram-negative Escherichia coli are model organisms used for the study of cell division in rod-shaped bacteria. Central component of cell division is a highly conserved, tubulin-like protein FtsZ, that forms a structure termed Z-ring at the future site of the septum. The Z-ring then serves as a scaffold for downstream division proteins (Fig. 1A). Two mechanisms were described having a negative effect on Z-ring assembly: nucleoid occlusion, which prevents division in the vicinity of the chromosome and Min system blocks, which blocks unwanted polar septation [reviewed in 1, 2]. The Min system acts by creating a concentration gradient of division inhibitor along the cell axis (Fig. 1B). The key component is MinC protein which prevents formation of Z-ring by inhibiting FtsZ polymerization and bundling of FtsZ protofilaments [reviewed in 3]. Activity of MinC and its recruitment to the cytoplasmic membrane is provided by interaction with MinD. MinC and MinD homologues are found in both model organisms, but specific action at polar sites is dependent on interaction with a third component termed topological determinant, that differs between E. coli and B. subtilis. MinE is the responsible protein in the E. coli system, while MinJ/DivIVA proteins are involved in B. subtilis. Behaviour of Min proteins in E. coli is highly dynamic and is based on a fine-tuned interaction between MinE and MinD, resulting in rapid oscillation of all Min proteins from one pole to another (Fig. 2), creating bipolar gradient of MinC. B. subtilis does not encode a homologue of MinE and the polar localization of MinCD is achieved by preferential attraction of MinCD complex to the cell poles via MinJ/DivIVA proteins (Fig. 3). DivIVA has an additional role, apart from the one in Min system – during sporulation, it ensures proper chromosome segregation, by interacting with a DNA-binding protein RacA. Clostridia are a diverse group of anaerobic bacteria and close relatives of Bacilli, that both belong to the phylum Firmicutes. Despite their historical designation as Gram-positive, a number of them has membrane organization characteristic of Gram-negative, combined with the ability to form endospores [3]. Clostridia were previously noticed for presence of homologues of both Min systems in their genomes [4, 5], however, their functionality and behaviour were not investigated. The combination of homologues from two systems, each characteristic for a Gram-positive or Gram-negative bacteria within genome of a single organism, leads us to speculate whether Clostridia could be relatives of a common ancestor of the two different cell membrane structures. The origin of the second membrane of Gram-negative bacteria is an unresolved question, on which many, even opposing theories exist. We have re-evaluated the presence of Min protein homologues in whole-genome sequences of selected Clostridia and found that many indeed contain genes of both systems. Additionally, we have looked more closely at protein interactions of Min systems between the pathogenic member Clostridium difficile and B. subtilis. Results Distribution of Min proteins homologues in Clostridia In the search of homologues of Min proteins we used the NCBI’s PSI-BLAST program [3] using a default threshold of 0.005. In the case of MinC, MinD, MinJ and DivIVA, sequences of B. subtilis PY79 proteins were used as reference, while for MinE homologues search, sequence of E. coli str. K-12 substr. MG1655 was utilized. Specific strains of Clostridia species were selected based on availability of their whole genome sequence. Results are summarized in Table 1. Fig.3: Measurements were performed in wild type and mutant strains carrying lacZ reporter fused to σF-specific promoter PspoIIQ. Activity of σFwas measured as specific enzyme activity in β-galactosidase assay. Negative control (NC) represents strain containing lacZ gene withouth this promoter.
5 µm
5 µm
(A)
(A)
(B)
(B)
(C)
(C)
Fig.1: A) Polymerization of FtsZ into Z-ring at the mid-cell. (
Fig.1: A) Polymerization of FtsZ into Z-ring at the mid-cell. (B) Gradient of MinC inhibitor formed along the cell axis.
(B)
(B)
(A)
(A)
MinC
MinC
FtsZ
FtsZ
Z-ring
Z-ring
Fig. 3: MinCDJ/DiviVA system in B. subtilis.
Fig. 3: MinCDJ/DiviVA system in B. subtilis.
chromosome
chromosome
Fig. 2: MinCDE system in E. coli.
Fig. 2: MinCDE system in E. coli.
Protein-protein interactions between MinD of C. difficile and M
Protein-protein interactions between MinD of C. difficile and Min proteins of B. subtilis as detected by BACTH Fusions of C. difficile MinD homologue (MinDCd) with T18 and T25 fragments of adenylate cyclase were constructed in the bacterial adenylate cyclase two-hybrid (BACTH) system [7; Fig. 4.]. MinCBs, MinDBs and MinJBs fusions in the BACTH system were prepared previously [5]. To test protein–protein interactions, the E. coli BTH101 strain (adenylate cyclase deficient) was co-transformed with various plasmid combinations and plated on LB plates supplemented with X-gal (40 µg.ml-1), IPTG (0.1 mM), ampicillin (100 µg.ml-1), and kanamycin (30 µg.ml-1) and grown for 24–72 h at 30 °C. β-galactosidase activity was measured as described in [8]. Conclusions Our analysis of selected clostridial genomes shows (Tab. 1), that as spore-formes, they contain DivIVA homologue and many also MinJ homologue. Whether this DivIVA serves as polar tether similarly as in B. subtilis Min system or only has role related to sporulation, remains unknown. Despite the absence of MinJ in some of the species, it is still possible that some other protein substitutes for the role of MinJ, and thus interconnects MinCD system with DivIVA. We found that MinDCd interacts with itself (Fig. 5), indicating a dimerization, which is confirmed in the case of MinDBs and MinDEc and which is important for MinC binding [9]. We have detected interaction of C. difficile MinDCd with all tested B. subtilis Min proteins – that is MinCBs, MinDBs, and MinJBs. Interaction of MinDCd and MinJBs is quite surprising, since we were unable to identify MinJ homologue in C. difficile genome. In B. subtilis, MinJ (also under name swrAB) forms an operon with a neighbouring gene swrAA, and it seems that the whole operon is missing in C. difficile (not shown). The functional characteristic of these homologues will be a subject of our future studies. Acknowledgements This work was supported by Grant 2/0009/13 from the Slovak Academy of Sciences and by a Grant from the Slovak Research and Development Agency under contract APVV-00335-10.
Fig. 5: Screening of protein-protein interactions between MinDC
Fig. 5: Screening of protein-protein interactions between MinDCd and Min proteins of B. subtilis compared to interactions amongst B. subtilis Min proteins.
Fig. 4: Principle of BACTH system - protein-protein interaction
Fig. 4: Principle of BACTH system - protein-protein interaction enables reconstitution of adenylate cyclase and thus expression of reporter gene lacZ, which metabolizes colorless X-gal substrate to blue indigo.
T18
T18
protein B
protein B
protein A
protein A
T25
T25
dibromo-dichloro- -indigo
dibromo-dichloro- -indigo
ATP
ATP
cAMP + CAP
cAMP + CAP
lacZ
lacZ
X-Gal
X-Gal
Table 1: Search for Min homologues in Clostridia. Numbers indic
Table 1: Search for Min homologues in Clostridia. Numbers indicate [%] of similarity/identity of amino acid sequence.
Escherichia coli K-12 substr. MG1655
Escherichia coli K-12 substr. MG1655
DIVIDER
.....................................................................................
DIVIDER copy
.....................................................................................
References
References
[1] Barák I., Wilkinson A. J. (2007) FEMS Microbiol. Rev. 31(3)
[1] Barák I., Wilkinson A. J. (2007) FEMS Microbiol. Rev. 31(3), pp. 311 [2] Wu L. J., Errington J. (2011) Nat. Rev. Microbiol. 10, pp. 8 [3] Yutin, N., and Galperin, M.Y. (2013) Environ Microbiol 15 (10), pp. 2631–2641 [4] Stragier, P. (2000) American Society for Microbiology, Washington, D. C., pp. 519-525 [5] Jamroškovič J., Pavlendová N., Muchová K. et al. (2012) Microbiology 158, pp. 1972
[6] Altschul, S.F., Madden, T.L., Schäffer, A.A. et al. (1997)
[6] Altschul, S.F., Madden, T.L., Schäffer, A.A. et al. (1997) Nucleic Acids Res 25, pp. 3389 3402 [7] Karimova, G., Pidoux, J., Ullmann, A. et al. (1998) Proc Natl Acad Sci USA 95, pp. 5752–5756 [8] Miller J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. [9] Wu, W., Park, K. T., Holyoak, T., et al. (2011. Mol microbiol 79(6), pp. 1515-1528
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