MamX encoded by the mamXY operon is involved in control of magnetosome maturation in Magnetospirillum gryphiswaldense MSR-1
- Jing Yang†1, 3,
- Shuqi Li†1, 3,
- Xiuliang Huang1, 3,
- Jinhua Li2, 3,
- Li Li1, 3,
- Yongxin Pan2, 3 and
- Ying Li1, 3Email author
© Yang et al.; licensee BioMed Central Ltd. 2013
Received: 2 July 2013
Accepted: 3 September 2013
Published: 11 September 2013
Magnetotactic bacteria produce membrane-enveloped magnetite crystals (magnetosomes) whose formation is controlled primarily by a gene island termed the magnetosome island (MAI). Characterization of single gene and operon function in MAI has elucidated in part the genetic basis of magnetosome formation. The mamX gene, located in the mamXY operon, is highly conserved in the MAI of all Magnetospirillum strains studied to date. Little is known regarding the function of mamX in the process of biomineralization.
A mamX deletion mutant (∆mamX) and its complemented strain (CmamX) by conjugation in M. gryphiswaldense strain MSR-1 were constructed. There were no striking differences in cell growth among ∆mamX, CmamX, and wild-type strain (WT). ∆mamX displayed a much weaker magnetic response than WT. Transmission electron microscopy revealed the presence of irregular, superparamagnetic magnetite particles in ∆mamX, in contrast to regular, single-domain particles in WT and CmamX. The phenotype of ∆mamX was similar to that of an ftsZ-like deleted mutant and mamXY operon deleted mutant reported previously. Quantitative real-time RT-PCR (qPCR) results indicated that the deletion of mamX had differential effects on the transcription levels of the other three genes in the operon.
The MamX protein plays an important role in controlling magnetosome size, maturation, and crystal form. The four MamXY proteins appear to have redundant functions involved in magnetosome formation. Our findings provide new insights into the coordinated function of MAI genes and operons in magnetosome formation.
KeywordsMagnetospirillum gryphiswaldense mamXY operon mamX Magnetosome Crystal maturation
Magnetotactic bacteria (MTB) produce nano-sized membrane-enveloped magnetic organelles termed magnetosomes, consisting of single-domain magnetite (Fe3O4) or greigite (Fe3S4) crystals that are integrated into one to several chains depending on the species [1, 2]. MTB are aquatic prokaryotes that utilize the magnetosomes to align themselves relative to magnetic fields and swim toward favorable low-oxygen, nutrient-rich environments. This behavior is called magneto-aerotaxis [1, 3].
Many studies over the past several decades have focused on the molecular mechanism of magnetosome formation and revealed several important facts. Magnetosome-related genes are concentrated in a structure called the “magnetosome island” (MAI) in the genomes of MTB [4, 5]. In Magnetospirillum strains such as M. gryphiswaldense MSR-1, M. magneticum AMB-1, and M. magnetotacticum MS-1, the MAI conservatively contains four common gene operons: mms6, mamGFDC, mamAB, and mamXY[2, 6]. The mamXY operon is also conserved in Magnetococcus sp. MC-1 . Mms6, a tightly bound protein found in the magnetosome membrane, plays an essential role in the control of magnetite crystallization and crystal size [8–10]. The MamGFDC proteins have partially redundant and collective functions in the control of magnetosome size . The mamAB operon is a large cluster containing most of the MTB-specific genes, including those that encode the proteins MamE (involved in the localization of magnetosome membrane protein [MMP]), MamK (actin-like protein involved in the alignment of magnetosome chains), and MamJ (interacts with MamK, an important factor in magnetosome chain formation) [12–15]. Recent studies have shown that the mamAB operon is necessary and sufficient for magnetite biomineralization [16, 17].
The mamXY operon received less attention than mms6, mamGFDC, and mamAB. mamXY is the last cluster in the MAI and contains four sequential genes termed mamY, mamX, mamZ, and ftsZ-like, identified as a polycistronic transcription unit . The MamXY proteins were shown to play crucial roles in magnetite biomineralization through whole operon deletion in MSR-1 . Such effect was less obvious in AMB-1 . MamY was reported to constrict the magnetosome membrane in AMB-1 . Deletion of FtsZ-like resulted in smaller superparamagnetic particles . MamZ has been predicted (without direct evidence to date) to be an ortholog of MamH and likely a permease belonging to the major facilitator superfamily. MamX has similarities to the serine-like proteases MamE and MamS, but there have been no systematic studies of its function to date. In view of the high conservation of mamXY in MTB, functional studies of this operon are needed to elucidate the entire MAI and its role in the mechanism of magnetosome formation. The present study is focused on the highly conserved but hitherto uncharacterized MamX protein.
Deletion of the mamXgene had no effect on cell growth
∆mamXshowed decreased intracellular iron content and magnetic response
The deletion of mamXresulted in irregular and smaller crystals
Magnetosome diameters and numbers in three MSR-1 strains
41.25 ± 10.46 a
15.35 ± 3.06 b
26.11 ± 9.92
20.85 ± 3.91
48.42 ± 11.82
6.55 ± 1.88
mamXY gene transcription levels were affected by mamXdeletion
Ratio of transcription levels of MamZ to other MamXY proteins in WT and Δ mamX strains, based on qPCR results
MamX is involved in magnetite crystal maturation in MSR-1 cells
To elucidate the function of the highly conserved MamX protein in MTB, we constructed mamX deletion mutant (∆mamX) and complemented (CmamX) strains of M. gryphiswaldense MSR-1. For ∆mamX, the Cmag value was zero and intracellular iron content was significantly reduced, although cell growth was similar to that of WT (Figure 1). HR-TEM observations revealed that the magnetite particles in ∆mamX were irregularly shaped, small (26.11±9.92 nm), and predominantly superparamagnetic, whereas those in WT were symmetrically cuboid, large (41.25±10.46 nm), and predominantly single-domain. These findings indicate that MamX plays an essential role in the control of magnetosome morphology and that mamX is involved in magnetite crystal maturation in MSR-1.
There was a notable reduction of intracellular iron content in ∆mamX, corresponding to a crystal diameter much smaller than that in WT. The observed alteration of the crystal lattice may account for the reduction of Cmag in ∆mamX and result in a phenotype similar to that of a mamXY operon knock-out in MSR-1 . Surprisingly, the mean crystal number per cell for ∆mamX (20.85±3.91) was 36% higher than that for WT (15.35±3.06). This finding may be due to the fact that crystals in the mutant strain were smaller; i.e., equivalent amounts of materials (iron, MMP, electrons, ATP, etc.) in the cells may have been capable of producing more crystals, as supported by HR-TEM observations (Figure 3E).
MamX has conserved double heme-binding motifs
MamX is conserved in not only spirillum strains such as M. gryphiswaldense MSR-1 (MGR_4149), M. magneticum AMB-1 (amb1017), and M. magnetotacticum MS-1 (MMMS1v1_36310026) but also in vibrio and cocci strains such as Magnetovibrio MV-1 (mv1g00028) and Magnetococcus sp. MC-1 (Mmc1_2238). A comparative genomic analysis showed that mamX is one of a set of 28 genes that are specifically associated with the magnetotactic phenotype . The ubiquity and specific presence of MamX within MTB suggest that this protein plays a role in magnetotaxis. The results of the present study indicate that MamX is involved in magnetite crystal maturation but do not clarify its exact function. A protein sequence blast search using PROSITE (http://prosite.expasy.org/) showed that MamX contains two CXXCH heme-binding motifs that are typical of c-type cytochromes (Additional file 1: Figure S1). Similar double heme-binding motifs were found recently in the magnetosome proteins MamE, MamP, and MamT [27, 28]. Site-directed mutagenesis of the two motifs in MamE resulted in the production of smaller magnetite crystals . These motifs were suggested to be involved in electron transport or as a redox buffer during magnetite formation . Such a function could explain the specific requirement of redox potential for magnetite formation in several MTB strains [29, 30] and may be related to the function of the double heme-binding motif in MamX.
The four proteins encoded by the mamXYoperon may have a close relationship
The qPCR results showed that the four genes in the mamXY operon were all highly expressed during the log phase of growth, supporting previous findings that the log phase is an essential period for MMP function and magnetosome synthesis . The expression of mamZ was much higher than that of the other three genes at each of the sampling times (Figure 5; Table 2), indicating that mamZ plays a crucial role during growth. MamZ is a highly hydrophobic protein with a predicted weight of 71.7 kDa and contains a major facilitator superfamily domain (predicted by PROSITE), a ferric reductase-like transmembrane component (Pfam; http://pfam.janelia.org/search), and up to 17 transmembrane helices (HMMTOP; http://www.enzim.hu/hmmtop). It is therefore possible that MamZ is involved in ferric iron reduction, although there is no direct experimental evidence to date for such a function. The results of the relative qPCR assay indicated that deletion of mamX resulted in a notable increase in mamY and ftsZ-like transcription but had no effect on mamZ transcription. These findings suggest some redundancy among the functions of mamX, mamY, and ftsz-like.
Application of the online tool STRING (http://string-db.org) predicted interactions among the four proteins encoded by the mamXY operon (Additional file 2: Figure S2). According to this predicted network view, the four MamXY proteins undergo intrinsic interactions with each other and are also associated with certain proteins related to cell division (MGR-2076, MGR-3226, MGR-1090, MGR-2217) and to cell wall formation (MGR-0063, MGR-1112, MGR-1092, MGR-2078, MGRGRv1-0136, MGRGRv1-0133) through FtsZ-like. These associated proteins in strain AMB-1 have predicted functions similar to those in MSR-1(Additional file 3: Table S1). Further experiments are needed to test this model.
Interestingly, the phenotypes of a mamX mutant, ftsZ-like mutant, and mamXY operon deleted mutant in MSR-1 are similar in that they produce magnetosomes that are small and irregularly shaped in comparison with those of WT [16, 18]. In view of the previous finding that MamGFDC proteins have partially redundant and collective functions in controlling magnetosome size , and the results of the present study, we propose that the four genes in the mamXY operon have redundant functions involved in the complex process of magnetosome formation. A recent study showed that a single deletion of the mamAB operon in MSR-1 resulted in the complete loss of magnetosome synthesis, whereas deletion of the conserved mms6, mamGFDC, and mamXY operons led to severe defects in the morphology, size, and organization of magnetite crystals . The MamP, MamS, MamR, and MamT proteins were shown to function in the regulation of crystal number, size, and shape . Magnetite biocrystallization in MTB is clearly a complex process in which many proteins are involved. It is appropriate now to consider completing the model of MMP functions and magnetosome formation that was proposed previously [14, 32].
The results of the present study show that the MamX protein plays an important role in controlling magnetosome size, maturation, and crystal form. Previous studies have shown that a single gene deletion in mamXY and knock-out of the entire operon result in very similar phenotypic characteristics. The MamXY proteins may therefore have redundant functions involved in magnetosome synthesis. These findings are important for further elucidation of the biomineralization process in MTB.
Bacterial strains and growth conditions
Strains and plasmids used in this study
Strains and plasmids
Source or reference
M. gryphiswaldense MSR-1
M. gryphiswaldense MSR-1 ΔmamX
mamX deficient mutant, Nxr Gmr
M. gryphiswaldense MSR-1 CmamX
complementation of ΔmamX, NxrGmrTcr
E. coli DH5α
endA1 hsdR17 (r- m+) supE44 thi-1 recA1 gyrA (NalR) recA1 Δ (lacZYA-argF)U169 deoR [Ø80ΔdlacZ ΔM15]
E. coli S17-1
thi endA recA hsdR with RP4-2-Tc::Mu-Km::Tn7 integrated in chromosome, Smr
pUC1918 carrying the aacC1 gene, Gmr
suicide vector for M. gryphiswaldense MSR-1, CmrTcr Ampr
pSUP202 derivative for mamX deletion, GmrCmrAmpr
Cloning vector, pRK290 derivative, Tcr
pRK415 derivative for mamX expression, Tcr
Construction of the mamXdeletion mutant and complemented strains
The mamX deletion mutant was constructed by conjugation and subsequent homologous recombination in MSR-1. (i) The 5′ flank (1003 bp; primers: mamX-5F, CGCGGATCCAT GTTGATGAACTTTGTCAA; mamX-5R,CGAGCTCGGGAGTTCGACTGTGGTCAA3) and 3′ flank (1043 bp; primers: mamX-3F, CGAGCTCGTGCCCTGCGTGACGACCAT; mamX-3R, ACGCGTCGACAACATTCCGAGCCAGATATA) of the mamX gene in the MSR-1 genome were amplified by PCR (restriction sites are underlined). The aacC1 gene that confers Gm resistance (Gmr) was digested from plasmid pUCGm by SacI sites. (ii) The digested and purified 5′ flank, Gmr, and 3′ flank were cloned into plasmid pSUP202 by BamHI, SacI, and Sal I sites to obtain the suicide plasmid pSUPpX2. (iii) E. coli strain S17-1 transformed with pSUPpX2 was conjugated with MSR-1 as described previously . The final Gmr CmS colonies, confirmed by PCR, comprised a double-crossover recombination mamX deletion mutant (∆mamX). To complement the mutant, the mamX gene (primers: X-F, 5′AACTGCAGTTGACCACAGTCGAACTCCC3′; X-R, 5′CGCGGATCCTATTCCATTG GGTGGGAGCG3′) was cloned into pRK415 by PstI and BamHI sites, and the resulting plasmid pRK415X was transferred into E. coli S17-1 (restriction sites are underlined). The subsequent conjugation was performed as described above. The Gmr Tcr colonies, confirmed by PCR, were complemented strains (termed CmamX).
Transmission electron microscopy
Cells were placed on a copper grid, washed twice with distilled water, dried, and observed by TEM (Philips Tecnai F30, Eindhoven, Netherlands). For HR-TEM (JEOL 2010, Tachikawa, Tokyo), a carbon grid was used.
Measurement of iron content
Each strain was cultured microaerobically at 30°C in OFM. After the cultures reached stationary phase, 10-ml samples were centrifuged at 10,000 x g for 2 min. The pellets were washed three times with distilled water, dried to a constant weight and nitrified in 1 ml nitric acid for 3 hr as described previously . Intracellular iron content was assayed using an Inductively Coupled Plasma Optical Emission Spectrometer (ICP-OES; Optima 5300DV; Perkin Elmer, Waltham, MA, USA). The iron percentage of cells was calculated as iron content divided by dry weight.
Rock magnetic measurements
Cell cultures were centrifuged (10,000 x g) at 4°C for 5 min, and the pellets were subjected to magnetic measurements. Room-temperature hysteresis loops and first-order reversal curves (FORCs) were measured by an Alternating Gradient Force Magnetometer Model MicroMag 2900 (Princeton Measurements Corp., Princeton, NJ, USA; sensitivity 1.0×10−11 Am2) as described previously .
Quantitative real-time RT-PCR(qPCR)
Total RNA was purified using TRIzol Reagent (Invitrogen Corp., Carlsbad, CA, USA) according to the manufacturer’s instructions. The remaining genomic DNA in RNA preparations was degraded by DNase I (Takara, Shiga, Japan). cDNA synthesis was performed using M-MLV reverse transcriptase, dNTPs, and random primers (Promega Corp., San Luis Obispo, CA, USA) according to the manufacturer’s instructions.
A LightCycler 480 Instrument II (Roche, South San Francisco, CA, USA) was used for qPCR. The LightCycler 480 SYBR Green I Master kit (Roche) was used as the manual. In a 20-μl PCR system, the template cDNA content was set below 500 ng and that of each oligo as 0.5 μM. The reaction program consisted of initial denaturation at 95°C for 10 min, followed by 40 cycles of denaturation at 95°C for 15 sec, annealing at 62°C for 5 sec, extension at 72°C for 15 sec, and fluorescence measurement at 76°C for 3 sec. The reactions were repeated three more times with template cDNA serially 10-fold diluted (1/10, 1/100, and 1/1000 concentrations) to ensure that the final cDNA concentrations were between 103 and 106 copies. The crossing point values (Cp) were converted to absolute copies of cDNA using standard curves. The relative expressions of the target genes were calculated by dividing the absolute number of copies of cDNA by that of the reference gene rpoc (which encodes RNA polymerase subunit ß') in the same batch reactions. The primer sequences for qPCR are listed in Additional file 4: Table S2.
High-resolution transmission electron microscopy
Magnetosome membrane protein
Quantitative real-time RT-PCR
Optimized flask medium
First-order reversal curves.
This study was supported by the National Natural Science Foundation of China (Grant No. 30970041 and 31270093) and the Undergraduate Student Innovation Program of China Agricultural University (Grant No. 2010-BKS-16). The authors thank Dr. Xin Gao (Testing Center, University of Science and Technology of China) for the HR-TEM observations, and Dr. S. Anderson for English editing of the manuscript.
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