A Large Gene Cluster Encoding Several Magnetosome Proteins Is Conserved in Different Species of Magnetotactic Bacteria

ABSTRACT In magnetotactic bacteria, a number of specific proteins are associated with the magnetosome membrane (MM) and may have a crucial role in magnetite biomineralization. We have cloned and sequenced the genes of several of these polypeptides in the magnetotactic bacterium Magnetospirillum gryphiswaldense that could be assigned to two different genomic regions. Except for mamA, none of these genes have been previously reported to be related to magnetosome formation. Homologous genes were found in the genome sequences ofM. magnetotacticum and magnetic coccus strain MC-1. The MM proteins identified display homology to tetratricopeptide repeat proteins (MamA), cation diffusion facilitators (MamB), and HtrA-like serine proteases (MamE) or bear no similarity to known proteins (MamC and MamD). A major gene cluster containing several magnetosome genes (including mamA and mamB) was found to be conserved in all three of the strains investigated. ThemamAB cluster also contains additional genes that have no known homologs in any nonmagnetic organism, suggesting a specific role in magnetosome formation.

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The Major Magnetosome Proteins MamGFDC Are Not Essential for Magnetite Biomineralization in Magnetospirillum gryphiswaldense but Regulate the Size of Magnetosome Crystals

Journal of Bacteriology ◽

10.1128/jb.01371-07 ◽

2007 ◽

Vol 190 (1) ◽

pp. 377-386 ◽

Cited By ~ 122

Author(s):

André Scheffel ◽

Astrid Gärdes ◽

Karen Grünberg ◽

Gerhard Wanner ◽

Dirk Schüler

Keyword(s):

Magnetotactic Bacteria ◽

Crystal Formation ◽

Wild Type ◽

Unknown Mechanism ◽

Magnetospirillum Gryphiswaldense ◽

Type Size ◽

Specific Proteins ◽

Magnetite Biomineralization ◽

Redundant Functions ◽

Small Hydrophobic

ABSTRACT Magnetospirillum gryphiswaldense and related magnetotactic bacteria form magnetosomes, which are membrane-enclosed organelles containing crystals of magnetite (Fe3O4) that cause the cells to orient in magnetic fields. The characteristic sizes, morphologies, and patterns of alignment of magnetite crystals are controlled by vesicles formed of the magnetosome membrane (MM), which contains a number of specific proteins whose precise roles in magnetosome formation have remained largely elusive. Here, we report on a functional analysis of the small hydrophobic MamGFDC proteins, which altogether account for nearly 35% of all proteins associated with the MM. Although their high levels of abundance and conservation among magnetotactic bacteria had suggested a major role in magnetosome formation, we found that the MamGFDC proteins are not essential for biomineralization, as the deletion of neither mamC, encoding the most abundant magnetosome protein, nor the entire mamGFDC operon abolished the formation of magnetite crystals. However, cells lacking mamGFDC produced crystals that were only 75% of the wild-type size and were less regular than wild-type crystals with respect to morphology and chain-like organization. The inhibition of crystal formation could not be eliminated by increased iron concentrations. The growth of mutant crystals apparently was not spatially constrained by the sizes of MM vesicles, as cells lacking mamGFDC formed vesicles with sizes and shapes nearly identical to those formed by wild-type cells. However, the formation of wild-type-size magnetite crystals could be gradually restored by in-trans complementation with one, two, and three genes of the mamGFDC operon, regardless of the combination, whereas the expression of all four genes resulted in crystals exceeding the wild-type size. Our data suggest that the MamGFDC proteins have partially redundant functions and, in a cumulative manner, control the growth of magnetite crystals by an as-yet-unknown mechanism.

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A Compass To Boost Navigation: Cell Biology of Bacterial Magnetotaxis

Journal of Bacteriology ◽

10.1128/jb.00398-20 ◽

2020 ◽

Vol 202 (21) ◽

Author(s):

Frank D. Müller ◽

Dirk Schüler ◽

Daniel Pfeiffer

Keyword(s):

Magnetic Field ◽

Cell Biology ◽

Molecular Mechanisms ◽

Magnetotactic Bacteria ◽

Genetically Engineered ◽

Model Organisms ◽

Complex Cell ◽

Magnetite Biomineralization ◽

Directed Motility ◽

The Impact

ABSTRACT Magnetotactic bacteria are aquatic or sediment-dwelling microorganisms able to take advantage of the Earth’s magnetic field for directed motility. The source of this amazing trait is magnetosomes, unique organelles used to synthesize single nanometer-sized crystals of magnetic iron minerals that are queued up to build an intracellular compass. Most of these microorganisms cannot be cultivated under controlled conditions, much less genetically engineered, with only few exceptions. However, two of the genetically amenable Magnetospirillum species have emerged as tractable model organisms to study magnetosome formation and magnetotaxis. Recently, much has been revealed about the process of magnetosome biogenesis and dedicated structures for magnetosome dynamics and positioning, which suggest an unexpected cellular intricacy of these organisms. In this minireview, we summarize new insights and place the molecular mechanisms of magnetosome formation in the context of the complex cell biology of Magnetospirillum spp. First, we provide an overview on magnetosome vesicle synthesis and magnetite biomineralization, followed by a discussion of the perceptions of dynamic organelle positioning and its biological implications, which highlight that magnetotactic bacteria have evolved sophisticated mechanisms to construct, incorporate, and inherit a unique navigational device. Finally, we discuss the impact of magnetotaxis on motility and its interconnection with chemotaxis, showing that magnetotactic bacteria are outstandingly adapted to lifestyle and habitat.

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Genetic organization and transcriptional analysis of a major gene cluster involved in siderophore biosynthesis in Pseudomonas putida WCS358.

Journal of Bacteriology ◽

10.1128/jb.170.4.1812-1819.1988 ◽

1988 ◽

Vol 170 (4) ◽

pp. 1812-1819 ◽

Cited By ~ 26

Author(s):

J D Marugg ◽

H B Nielander ◽

A J Horrevoets ◽

I van Megen ◽

I van Genderen ◽

...

Keyword(s):

Pseudomonas Putida ◽

Gene Cluster ◽

Major Gene ◽

Transcriptional Analysis ◽

Genetic Organization ◽

Siderophore Biosynthesis

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Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the Alphaproteobacteria

mSystems ◽

10.1128/msystems.00315-19 ◽

2019 ◽

Vol 4 (5) ◽

Cited By ~ 2

Author(s):

Haijian Du ◽

Wenyan Zhang ◽

Wensi Zhang ◽

Weijia Zhang ◽

Hongmiao Pan ◽

...

Keyword(s):

Gene Duplication ◽

Gene Cluster ◽

Geomagnetic Field ◽

Evolutionary Biology ◽

Genomic Analysis ◽

Magnetotactic Bacteria ◽

Duplication Event ◽

Comparative Genomic ◽

Content Type ◽

Evolutionary Trajectories

ABSTRACT The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. IMPORTANCE A diversity of organisms can sense the geomagnetic field for the purpose of navigation. Magnetotactic bacteria are the most primitive magnetism-sensing organisms known thus far and represent an excellent model system for the study of the origin, evolution, and mechanism of microbial magnetoreception (or magnetotaxis). The present study is the first report focused on magnetosome gene cluster duplication in the Alphaproteobacteria, which suggests the important role of gene duplication in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. A novel scenario for the evolution of magnetotaxis in the Alphaproteobacteria is proposed and may provide new insights into evolution of magnetoreception of higher species.

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Albicidin Pathotoxin Produced by Xanthomonas albilineans Is Encoded by Three Large PKS and NRPS Genes Present in a Gene Cluster Also Containing Several Putative Modifying, Regulatory, and Resistance Genes

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2004.17.4.414 ◽

2004 ◽

Vol 17 (4) ◽

pp. 414-427 ◽

Cited By ~ 43

Author(s):

Monique Royer ◽

Laurent Costet ◽

Eric Vivien ◽

Martine Bes ◽

Arnaud Cousin ◽

...

Keyword(s):

Gene Cluster ◽

Resistance Genes ◽

Major Gene ◽

In Silico Analysis ◽

Toxin Production ◽

Structural Features ◽

Open Reading Frames ◽

Modular Architecture ◽

Large Genes ◽

Xanthomonas Albilineans

Xanthomonas albilineans, which causes leaf scald disease of sugarcane, produces a highly potent pathotoxin called albicidin. We report here sequencing and homology analysis of the major gene cluster, XALB1 (55,839 bp), and a second, smaller region, XALB2 (2,986 bp), involved in albicidin biosynthesis. XALB1 contains 20 open reading frames, including i) three large genes with a modular architecture characteristic of polyketide synthases (PKSs) and nonribosomal peptide synthases (NRPSs) and ii) several putative modifying, regulatory, and resistance genes. Sequencing and complementation studies of six albicidin-defective mutants enabled us to confirm the involvement of the three PKS and NRPS genes encoded by XALB1 in albicidin production. XALB2 contains only one gene that is required for post-translational activation of PKS and NRPS enzymes, confirming the involvement of these enzymes in albicidin biosynthesis. In silico analysis of these three PKS or NRPS enzymes allowed us to propose a model for the albicidin backbone assembly and to gain insight into the structural features of this pathotoxin. This is the first description of a complete mixed PKS—NRPS gene cluster for toxin production in the genus Xanthomonas.

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The Acidic Repetitive Domain of the Magnetospirillum gryphiswaldense MamJ Protein Displays Hypervariability but Is Not Required for Magnetosome Chain Assembly

Journal of Bacteriology ◽

10.1128/jb.00421-07 ◽

2007 ◽

Vol 189 (17) ◽

pp. 6437-6446 ◽

Cited By ~ 68

Author(s):

André Scheffel ◽

Dirk Schüler

Keyword(s):

Electron Tomography ◽

Direct Interaction ◽

Magnetotactic Bacteria ◽

Central Domain ◽

Magnetospirillum Gryphiswaldense ◽

Binding Domains ◽

Cytoskeletal Filament ◽

Distinct Sequence ◽

Specific Proteins ◽

Two Hybrid

ABSTRACT Magnetotactic bacteria navigate along the earth's magnetic field using chains of magnetosomes, which are intracellular organelles comprising membrane-enclosed magnetite crystals. The assembly of highly ordered magnetosome chains is under genetic control and involves several specific proteins. Based on genetic and cryo-electron tomography studies, a model was recently proposed in which the acidic MamJ magnetosome protein attaches magnetosome vesicles to the actin-like cytoskeletal filament formed by MamK, thereby preventing magnetosome chains from collapsing. However, the exact functions as well as the mode of interaction between MamK and MamJ are unknown. Here, we demonstrate that several functional MamJ variants from Magnetospirillum gryphiswaldense and other magnetotactic bacteria share an acidic and repetitive central domain, which displays an unusual intra- and interspecies sequence polymorphism, probably caused by homologous recombination between identical copies of Glu- and Pro-rich repeats. Surprisingly, mamJ mutant alleles in which the central domain was deleted retained their potential to restore chain formation in a ΔmamJ mutant, suggesting that the acidic domain is not essential for MamJ's function. Results of two-hybrid experiments indicate that MamJ physically interacts with MamK, and two distinct sequence regions within MamJ were shown to be involved in binding to MamK. Mutant variants of MamJ lacking either of the binding domains were unable to functionally complement the ΔmamJ mutant. In addition, two-hybrid experiments suggest both MamK-binding domains of MamJ confer oligomerization of MamJ. In summary, our data reveal domains required for the functions of the MamJ protein in chain assembly and maintenance and provide the first experimental indications for a direct interaction between MamJ and the cytoskeletal filament protein MamK.

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Exogenous or l-Rhamnose-Derived 1,2-Propanediol Is Metabolized via a pduD-Dependent Pathway in Listeria innocua

Applied and Environmental Microbiology ◽

10.1128/aem.01074-08 ◽

2008 ◽

Vol 74 (22) ◽

pp. 7073-7079 ◽

Cited By ~ 17

Author(s):

Junfeng Xue ◽

Charles M. Murrieta ◽

Daniel C. Rule ◽

Kurt W. Miller

Keyword(s):

Gene Cluster ◽

Listeria Innocua ◽

Large Gene ◽

Diol Dehydratase ◽

Dependent Pathway

ABSTRACT 1,2-Propanediol (1,2-PD) added exogenously to cultures or produced endogenously from l-rhamnose is metabolized to n-propanol and propionate in Listeria innocua Lin11. The pduD gene, which encodes a diol dehydratase ß subunit homolog, is required for 1,2-PD catabolism. pduD and 16 other genes within the pduA-to-pduF region of a large gene cluster are induced in medium containing 1,2-PD.

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