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Journal of Bacteriology, June 2000, p. 3305-3309, Vol. 182, No. 11
Department of Biochemistry, Michigan State
University, East Lansing, Michigan 48824
Received 31 January 2000/Accepted 14 March 2000
Processing of pro- The sporulation process of
Bacillus subtilis has proven to be an excellent system
for discovering novel gene regulatory mechanisms and elucidating
their role in temporal and spatial control of gene expression (14,
34). Sporulation involves the formation of an asymmetrically
positioned septum that divides the developing cell into a larger mother
cell compartment and a smaller forespore. Both cell types receive a
copy of the genome, and differential gene expression, controlled
primarily by the activation of new
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Evidence that SpoIVFB Is a Novel Type of Membrane
Metalloprotease Governing Intercompartmental Communication during
Bacillus subtilis Sporulation
ABSTRACT
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Abstract
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References
K in the mother cell compartment
of sporulating Bacillus subtilis involves SpoIVFB and is
governed by a signal from the forespore. SpoIVFB has an HEXXH motif
characteristic of metalloproteases embedded in one of its transmembrane
segments. Several conservative single amino acid changes in the HEXXH
motif abolished function. However, changing the glutamic acid residue to aspartic acid, or changing the isoleucine residue that precedes the
motif to proline, permitted SpoIVFB function. Only one other putative
metalloprotease, site 2 protease has been shown to tolerate aspartic
acid rather than glutamic acid in its HEXXH sequence. Site 2 protease
and SpoIVFB share a second region of similarity with a family of
putative membrane metalloproteases. A conservative change in this
region of SpoIVFB abolished function. Interestingly, SpoIVFA increased
the accumulation of certain mutant SpoIVFB proteins but was unnecessary
for accumulation of wild-type SpoIVFB.
TEXT
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Abstract
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References
subunits of RNA
polymerase (RNAP), drives a series of morphological changes. The mother
cell side of the septum engages in a phagocytic-like process called
engulfment, which results in the forespore being wholly surrounded by
two membranes within the mother cell (Fig. 1). Completion of engulfment triggers
activation of G in the forespore (12, 16).
Transcription by G RNAP of the spoIVB gene
initiates a signaling pathway that governs processing of
pro-K to its active form in the mother cell (3,
22) (Fig. 1). K directs transcription of genes
whose products drive further morphogenesis, including the formation of
cortex and coat layers, which encapsulate the forespore, and lysis of
the mother cell to release the mature spore (3, 9, 11, 13,
42-44).
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FIG. 1.
Model showing proteins involved in the signal
transduction pathway that governs pro- K processing. The
top part shows a sporangium in which engulfment of the forespore (FS)
has been completed. Dots represent pro-K associated with
the mother cell (MC) membrane and the outermost membrane surrounding
the FS (39). Triangles represent SpoIVFA and SpoIVFB
associated with the outermost membrane surrounding the FS
(26). The bottom part shows an expanded view of the two
membranes surrounding the FS. The topologies depicted for BofA,
SpoIVFA, and SpoIVFB are based on analysis of lacZ
and phoA fusions in E. coli (8, 35).
The HELGH and DG sequences of SpoIVFB subjected to mutational
analysis appear to be in transmembrane segments. The model depicts the
hydrophobic prosequence of pro-K (13, 33)
inserted into the outermost membrane surrounding the FS, but it is not
known how pro-K associates with membranes
(39). Cleavage of pro-K releases
K into the MC, where it binds core RNAP and directs
transcription.
This study was aimed at elucidating the mechanism of
pro-K processing. Pro-K has 20 N-terminal
amino acids that are removed by processing during sporulation
(13). This processing step serves as a developmental checkpoint, coupling events in the forespore to K
activation in the mother cell (4, 18). It delays the
appearance of active K by about 1 h. If the
checkpoint is circumvented and K accumulates earlier
than normal, sporulation efficiency drops (4), perhaps owing
to a K-dependent feedback loop that inhibits production
of early mother cell transcription factors (40, 41). Genetic
studies identified components involved in the checkpoint and led to the
following model: SpoIVFB was proposed to be the protease that
processes pro-K, or a positive regulator of such a
protease (5), and SpoIVFA and BofA appeared to be
negative regulators of processing until a signal from the
forespore relieved this inhibition (5, 27, 28). (Fig. 1).
SpoIVFB and SpoIVFA are membrane proteins that appear to
be localized to the outermost membrane surrounding the forespore
(8, 26). BofA is also a membrane protein (35), and recent results suggest that it stabilizes SpoIVFA, which
may be the primary inhibitor of SpoIVFB (25). Consistent
with the idea that SpoIVFB is the processing enzyme, it
enhanced processing when coproduced with pro-K in
growing B. subtilis or Escherichia coli, although
the amount of processing was small (17). It was noted that
SpoIVFB has a sequence (VLIHELGHAA) matching a motif
found in zinc-dependent endopeptidases (17), but hydropathy
analysis had suggested this sequence is embedded in a
transmembrane domain (5) (Fig. 1), and no metalloproteases
with an HEXXH motif in a membrane-spanning segment had been described.
Several findings motivated us to test the idea that SpoIVFB is a
metalloprotease. First, Rawson et al. (24) described the human site 2 protease (S2P), which has an essential HEIGH sequence embedded within or near the surface of the endoplasmic reticulum (38) and is proposed to mediate intramembrane cleavage of
sterol regulatory element-binding proteins (6), releasing
these transcription factors from the endoplasmic reticulum and
permitting regulation of genes involved in cholesterol and fatty acid
metabolism (2). Second, pro-K was shown to be
membrane associated (39) (Fig. 1). This suggested that
pro-K, like sterol regulatory element-binding proteins,
might be cleaved within a membrane or near its surface and that
SpoIVFB might be functionally homologous to S2P (14).
Third, a SpoIVFB-green fluorescent protein chimera appeared to
accumulate to a higher level than native SpoIVFB when produced in
growing B. subtilis, and more pro-K
processing was observed, strengthening the hypothesis that SpoIVFB is the processing enzyme (27).
Here, we present mutational evidence that SpoIVFB is a metalloprotease. While this work was in progress, computer database searching and protein multiple sequence alignment identified SpoIVFB and S2P as members of a novel clan of putative zinc metallopeptidases (15, 29). Also, using a strategy different than the one we employed, Rudner et al. (29) analyzed the effect of mutations in spoIVFB. Our results confirm and extend those of Rudner et al. (29), providing additional insights into the requirements for SpoIVFB function.
Rescue of pro-K processing and sporulation by a
plasmid bearing spoIVFB.
To develop a system for mutational
analysis of spoIVFB, an autonomously replicating plasmid
containing the spoIVFB gene fused to the
isopropyl-
-D-thiogalactopyranoside-inducible
spac promoter was constructed. A 1.0-kbp
HindIII-SalI fragment containing the spoIVFB gene from pSC227 (19) was ligated to
HindIII-SalI-digested pDG148
(32), resulting in pSL16. This plasmid was transformed (1) into B. subtilis OR745 (26), which
lacks the chromosomal spoIVFB gene, and into B. subtilis BSL51 (19), which lacks both spoIVFA and spoIVFB. Transformants were selected
on Luria-Bertani agar (30) containing kanamycin sulfate (5 µg/ml). Figure 2 shows that pSL16, but
not the empty vector from which it was derived (pDG148), allowed
production of K during sporulation. The level of
K that accumulated was comparable in the strains with
(lane 5) or without (lane 3) spoIVFA but significantly less
than in wild-type PY79 (37) (lane 1). The level of
K did not increase in pSL16-containing strains harvested
1 h later during sporulation (i.e., at T6
[data not shown]), suggesting that pro-K processing
was not merely delayed relative to that in wild-type cells. Since it
was known that very little K is needed for spore
formation (19), we measured the sporulation efficiency of
the pSL16-containing strains. Table 1
shows that OR745/pSL16 and BSL51/pSL16 formed heat-resistant spores
nearly as efficiently as wild-type cells and several orders of
magnitude more efficiently than negative control strains containing
pDG148. These results demonstrate that pSL16 can partially rescue
pro-K processing and sporulation of spoIVFB
mutant cells in the presence (OR745) or absence (BSL51) of
spoIVFA and that the sporulation assay in particular is a
sensitive test for SpoIVFB function.
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Mutational analysis of the HEXXH motif. To test the hypothesis that SpoIVFB is a metalloprotease (17), we made mutations in and around the HELGH sequence at positions 43 to 47 (Fig. 1). Plasmids with a mutation resulting in an I42P, E44A, E44D, or E44Q substitution in SpoIVFB were derived from pSL16 using the QuickChange site-directed mutagenesis kit (Stratagene); such plasmids are referred to herein as, e.g., pSL16 I42P. Plasmids with a mutation resulting in an H43F or H47F substitution were created using a sequence overlap extension strategy to synthesize full-length spoIVFB with the desired mutation, followed by subcloning into HindIII-SalI-digested pDG148 to construct plasmids otherwise identical to pSL16. Details of the sequence overlap extension procedure and primer sequences can be found at our web site (http: //www.bch.msu.edu/faculty/kroos.htm). Each mutant spoIVFB allele was completely sequenced to ensure that no additional mutations had been introduced.
In zinc metallopeptidases, the two histidine residues of the HEXXH motif coordinate zinc, and the glutamic acid residue promotes nucleophilic attack by a water molecule on the carbonyl atom of the substrate peptide bond (23). If SpoIVFB is a metalloprotease, then changing the histidine residues to phenylalanine was predicted to prevent metal binding and cause loss of function. Changing the putative catalytic glutamic acid residue to glutamine or alanine was also expected to cause loss of function. Table 1 shows that these predictions were met. The H43F, E44A, E44Q, and H47F changes each abolished the ability of pSL16 to restore sporulation of OR745 or BSL51. To determine whether the mutant proteins accumulate, we performed Western blot analysis with antibodies against SpoIVFB. Figure 3A shows that the mutant SpoIVFB proteins, with the exception of the H43F mutant, accumulated during sporulation of OR745 to a level comparable to that of wild-type SpoIVFB produced from pSL16 or from the chromosome (PY79); however, in BSL51 (lacking spoIVFA) the mutant SpoIVFB proteins did not accumulate to a detectable level, whereas wild-type SpoIVFB was detected (Fig. 3B). OR745 containing pSL16 with any of the mutant spoIVFB alleles failed to process pro-K (data not shown). These results demonstrate the
critical nature of the HEXXH motif for SpoIVFB function and
strongly support the idea that SpoIVFB is a metalloprotease, in
agreement with the findings of Rudner et al. (29). The
absence of detectable mutant SpoIVFB proteins in BSL51 indicates
that SpoIVFA is more critical for accumulation of the mutant
proteins than it is for the wild-type protein.
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K
processing during sporulation of OR745. These results demonstrate that
SpoIVFB, like S2P but unlike cytoplasmic metalloproteases, tolerates the E-to-D change in its HEXXH sequence, supporting the idea
that SpoIVFB and S2P belong to a novel class of metalloproteases (14, 15, 29). Perhaps these proteins have greater
conformational flexibility in the region of the HEXXH motif owing to
its presence in a membrane (8, 38). During catalysis, the
acidic amino acid residue must be accessible to a water molecule if the
mechanism of peptide bond cleavage by SpoIVFB and S2P is like that
of well-studied metalloproteases (23). Interestingly, pSL16
E44D did not restore heat-resistant spore formation to BSL51 when
sporulation was induced in liquid (Table 1), and the mutant protein was
undetectable (Fig. 3B), whereas it accumulated in OR745/pSL16 E44D
(Fig. 3A). Thus, SpoIVFA is more important for accumulation of
SpoIVFB E44D than it is for accumulation of wild-type SpoIVFB.
However, BSL51/pSL16 E44D colonies turned faint brown on Difco
sporulation medium (DSM) agar, whereas BSL51 colonies remained cream
colored. Brown pigmentation is caused by expression of cotA
(31), a K-dependent gene (43),
suggesting that SpoIVFB E44D can function weakly under these
conditions. Microscopic examination suggested the presence of more
spores in colonies of BSL51 with pSL16 E44D than without the plasmid,
and this was confirmed by sporulation assays of samples from the
colonies, with BSL51/pSL16 E44D and BSL51 showing about 10 and
10
4% sporulation efficiency, respectively, after 2 days
at 37°C.
Changing isoleucine at position 42 to proline had an effect very
similar to that of the E44D substitution. pSL16 I42P rescued sporulation (Table 1) and partially restored pro-K
processing (Fig. 2, lane 6) of OR745. These results are novel. In
metalloproteases of known structure, the HEXXH motif is embedded in an
-helix (23). Proline is disruptive of -helical
structure and is not found at the position preceding the HEXXH
motif in known metalloproteases (23). The ability to
tolerate proline in this position may be a unique feature of
metalloproteases that have the HEXXH motif in a transmembrane segment.
Proline may be less disruptive of -helical structure in the
hydrophobic environment of the lipid bilayer, and in SpoIVFB the
sequence preceding and including the HEXXH motif (LLCLLLIVLIHELGH)
(5) strongly favors an -helical structure, which the
proline substitution may perturb only slightly. It would be very
interesting to substitute proline for valine at the position preceding
the HEXXH motif in S2P (24) to see whether the analogy with
SpoIVFB can be extended and whether the ability to function with
proline at this position might be a general feature of this family of
putative membrane metalloproteases (15, 29). Like
SpoIVFB E44D, SpoIVFB I42P failed to accumulate to a detectable
level in BSL51/pSL16 I42P (Fig. 3B), and this strain failed to
sporulate in liquid (Table 1), whereas the mutant protein
accumulated to the wild-type level in OR745/pSL16 I42P (Fig. 3A).
Also, BSL51/pSL16 I42P exhibited an oligosporogenous phenotype
similar to that of BSL51/pSL16 E44D on DSM agar, indicative of the weak
but significant function of SpoIVFB I42P in the absence of SpoIVFA.
Mutational analysis of a second conserved region of SpoIVFB. A BLAST search with the SpoIVFB sequence identified significant similarity to several hypothetical proteins of unknown function that had been discovered as a result of archaea genome sequencing projects (data not shown). These sequences contained an HEXXH motif and a second conserved region containing the sequence DG. To test the importance of this sequence in SpoIVFB, we made mutations that changed the aspartic acid residue at position 137 (Fig. 1). While this work was in progress, Lewis and Thomas (15) published the results of iterative BLAST searches with the S2P sequence, which identified a novel clan of putative zinc metalloproteases, including SpoIVFB. They called the conserved region containing the DG sequence region C and identified a consensus sequence. Computer analysis by Rudner et al. (29) also identified this region, which they called the NPDG motif, and they performed mutational analysis of this region. We constructed plasmids with a mutation resulting in a D137H or D137N substitution in SpoIVFB using the QuickChange site-directed mutagenesis kit (Stratagene) with pSL16 as the template. Plasmids with a mutation resulting in a D137A or D137E substitution were created using a sequence overlap extension strategy as described above. Details of the sequence overlap extension procedure and primer sequences can be found at our web site (http: //www.bch.msu.edu/faculty/kroos.htm). Each mutant spoIVFB allele was completely sequenced to ensure that no additional mutations had been introduced.
Replacement of the aspartic acid at position 137 of SpoIVFB with alanine, glutamic acid, histidine, or asparagine abolished sporulation rescue of OR745 or BSL51 (Table 1). OR745 containing pSL16 with any of these mutant spoIVFB alleles failed to process pro-K (data not shown). Of these
mutant proteins, only SpoIVFB D137N accumulated to a detectable
level during sporulation, and unlike all the other mutant proteins we
tested, SpoIVFB D137N accumulated to about the same level as
wild-type SpoIVFB in the presence or absence of SpoIVFA (Fig.
3). We conclude, in agreement with the findings of Rudner et al.
(29), that a conservative change of the aspartic acid at
position 137 of SpoIVFB to asparagine abolishes function. The same
change in the corresponding region of S2P has been shown to abolish
function (38). Since the DG sequence is conserved in
all putative metalloproteases belonging to the family that includes
SpoIVFB and S2P (15, 29), it is likely to be important
for the function of all members of the clan. It has been speculated
that the aspartic acid residue is a zinc ligand (15, 29,
38), since metalloproteases typically coordinate zinc with the
two histidine residues of the HEXXH motif and a third ligand
(23).
Role of SpoIVFA in accumulation of SpoIVFB.
SpoIVFA has been proposed to stabilize thermolabile SpoIVFB
during sporulation, based on the finding that an in-frame deletion in
spoIVFA greatly reduces sporulation at 37°C but not at
30°C (5, 8). We observed no significant difference in the
sporulation efficiency at 37°C of OR745 (expressing
spoIVFA from the chromosome) and BSL51 (lacking
spoIVFA) containing pSL16 (Table 1), and the sporulation
efficiency of BSL51/pSL16 did not increase at 30°C (data not shown).
The altered timing and/or the increased level of SpoIVFB production
from pSL16 appears to make SpoIVFA dispensable for sporulation at
37°C. However, production of SpoIVFB from pSL16 was not optimal
for rescue of pro-K processing (Fig. 2). Perhaps
spoIVFB must be expressed in cis with
spoIVFA and/or the two proteins must be produced at a
certain stoichiometric ratio to function optimally. Resnekov
(25) recently reported that spoIVFA must be
expressed in cis with spoIVFB-gfp in order to
allow a SpoIVFB-green fluorescent protein chimera to accumulate
more abundantly in B. subtilis engineered to produce these
proteins during growth (27).
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ACKNOWLEDGMENTS |
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We thank S. Lu for constructing pSL16 and pSL28a. We thank D. Green, S. Cutting, D. Rudner, P. Fawcett, R. Losick, and O. Resnekov for communicating results prior to publication. We are grateful to D. Rudner for encouraging us to use OR745 and for sending the strain, and we are grateful to O. Resnekov for the SpoIVFB antibody affinity purification protocol.
This research was supported by the Michigan Agricultural Experiment Station and by grant GM43585 from the National Institutes of Health.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Biochemistry, Michigan State University, East Lansing, MI 48824. Phone: (517) 355-9726. Fax: (517) 353-9334. E-mail: kroos{at}pilot.msu.edu.
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