Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity

Montanini, Barbara; Blaudez, Damien; Jeandroz, Sylvain; Sanders, Dale; Chalot, Michel

doi:10.1186/1471-2164-8-107

Cited by 372 publications

(474 citation statements)

References 57 publications

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“…Whereas MamP was implicated in the control of magnetite crystal size and number, MamE is thought to be involved in magnetosome formation by directing the proper localization of a subset of magnetosome proteins (10). MamM and MamB share homology with cation diffusion facilitator (CDF) transporters (34,35) and are assumed to mediate iron transport into the magnetosome compartment (8). Multiple sequence comparisons were performed with all identified Mam homologs of Mbav to analyze their phylogenetic relation to magnetosome proteins from other MTB (Figs.…”

Section: Resultsmentioning

confidence: 99%

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Jogler

Wanner

Kolinko

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

108

172

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Magnetotactic bacteria (MTB) are a phylogenetically diverse group which uses intracellular membrane-enclosed magnetite crystals called magnetosomes for navigation in their aquatic habitats. Although synthesis of these prokaryotic organelles is of broad interdisciplinary interest, its genetic analysis has been restricted to a few closely related members of the Proteobacteria, in which essential functions required for magnetosome formation are encoded within a large genomic magnetosome island. However, because of the lack of cultivated representatives from other phyla, it is unknown whether the evolutionary origin of magnetotaxis is monophyletic, and it has been questioned whether homologous mechanisms and structures are present in unrelated MTB. Here, we present the analysis of the uncultivated "Candidatus Magnetobacterium bavaricum" from the deep branching Nitrospira phylum by combining micromanipulation and whole genome amplification (WGA) with metagenomics. Target-specific sequences obtained by WGA of cells, which were magnetically collected and individually sorted from sediment samples, were used for PCR screening of metagenomic libraries. This led to the identification of a genomic cluster containing several putative magnetosome genes with homology to those in Proteobacteria. A variety of advanced electron microscopic imaging tools revealed a complex cell envelope and an intricate magnetosome architecture. The presence of magnetosome membranes as well as cytoskeletal magnetosome filaments suggests a similar mechanism of magnetosome formation in "Cand. M. bavaricum" as in Proteobacteria. Altogether, our findings suggest a monophyletic origin of magnetotaxis, and relevant genes were likely transferred horizontally between Proteobacteria and representatives of the Nitrospira phylum.M agnetotactic bacteria (MTB) are widespread aquatic microorganisms that use unique intracellular organelles called magnetosomes to navigate along the earth's magnetic field while searching for growth-favoring microoxic zones within stratified sediments. In strains of Magnetospirillum, it was shown that magnetosomes consist of magnetite (Fe 3 O 4 ) crystals enclosed by a dedicated phospholipid membrane. The magnetosome membrane (MM) contains a specific set of proteins (1-3), which direct the biomineralization of highly ordered crystals along actin-like cytoskeletal filaments that control the assembly and intracellular positioning of a linear magnetosome chain (4-7). Synthesis of magnetosomes has recently emerged as a model for prokaryotic organelle formation and biomineralization (8-11). The trait of magnetotaxis is widely spread among Proteobacteria including members from the α-, δ-and γ-subdivisions, as well as uncultivated species from the deep branching Nitrospira phylum (8). The presence of MTB within unrelated lines of various phylogenetic groups, as well as their stunning diversity with respect to magnetosome shape, composition, and intracellular organization lead to speculations of whether the evolutionary origin of magnetota...

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Section: Resultsmentioning

confidence: 99%

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Jogler

Wanner

Kolinko

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

108

172

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“…The Two Conserved Hydrophilic Amino Acid Residues in TMs II and V of hZnT6 Are Not Involved in the Zinc-binding SiteMany CDF/ZnT proteins form homo-oligomers with the zincbinding site being formed by four conserved hydrophilic residues (2ϫ Asp and 2ϫ His in vertebrates) present in TMs II and V (12,23) (Fig. 1).…”

Section: Znt6mentioning

confidence: 99%

“…Information obtained from a number of mutagenesis studies has shown that the zinc-binding site embedded in the TM domains (TMDs) is essential for zinc transport across the cellular membrane by the CDF/ZnT proteins, suggesting that this may be true for all of the CDF/ZnT homo-oligomers (reviewed in Ref. 23).…”

mentioning

confidence: 99%

Demonstration and Characterization of the Heterodimerization of ZnT5 and ZnT6 in the Early Secretory Pathway

Fukunaka

Suzuki

Kurokawa

et al. 2009

Journal of Biological Chemistry

104

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The majority of CDF/ZnT zinc transporters form homooligomers. However, ZnT5, ZnT6, and their orthologues form hetero-oligomers in the early secretory pathway where they load zinc onto zinc-requiring enzymes and maintain secretory pathway functions. The details of this hetero-oligomerization remain to be elucidated, and much more is known about homo-oligomerization that occurs in other CDF/ZnT family proteins. Here, we addressed this issue using co-immunoprecipitation experiments, mutagenesis, and chimera studies of hZnT5 and hZnT6 in chicken DT40 cells deficient in ZnT5, ZnT6, and ZnT7 proteins. We found that hZnT5 and hZnT6 combine to form heterodimers but do not form complexes larger than heterodimers. Mutagenesis of hZnT6 indicated that the sites present in transmembrane domains II and V in which many CDF/ZnT proteins have conserved hydrophilic amino acid residues are not involved in zinc binding of hZnT6, although they are required for zinc transport in other CDF/ZnT family homo-oligomers. We also found that the long N-terminal half of hZnT5 is not necessary for its functional interaction with hZnT6, whereas the cytosolic C-terminal tail of hZnT5 is important in determining hZnT6 as a partner molecule for heterodimer formation. In DT40 cells, cZnT5 variant lacking the N-terminal half was endogenously induced during periods of endoplasmic reticulum stress and so seemed to function to supply zinc to zincrequiring enzymes under these conditions. The results outlined here provide new information about the mechanism of action through heterodimerization of CDF/ZnT proteins that function in the early secretory pathway.

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“…This protein increased Mn tolerance and accumulation when expressed in yeast or Arabidopsis (13). The CDF gene family is phylogenetically very widely distributed with representatives in bacteria, yeast, plants, and humans (20,21). The encoded transporters are powered by H ϩ or K ϩ antiport (22).…”

mentioning

confidence: 99%

A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance

Peiter

Montanini

Gobert

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

253

262

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Manganese toxicity is a major problem for plant growth in acidic soils, but cellular mechanisms that facilitate growth in such conditions have not been clearly delineated. Established mechanisms that counter metal toxicity in plants involve chelation and cytoplasmic export of the metal across the plasma or vacuolar membranes out of the cell or sequestered into a large organelle, respectively. We report here that expression of the Arabidopsis and poplar MTP11 cation diffusion facilitators in a manganesehypersensitive yeast mutant restores manganese tolerance to wild-type levels. Microsomes from yeast expressing AtMTP11 exhibit enhanced manganese uptake. In accord with a presumed function of MTP11 in manganese tolerance, Arabidopsis mtp11 mutants are hypersensitive to elevated levels of manganese, whereas plants overexpressing MTP11 are hypertolerant. In contrast, sensitivity to manganese deficiency is slightly decreased in mutants and increased in overexpressing lines. Promoter-GUS studies showed that AtMTP11 is most highly expressed in root tips, shoot margins, and hydathodes, but not in epidermal cells and trichomes, which are generally associated with manganese accumulation. Surprisingly, imaging of MTP11-EYFP fusions demonstrated that MTP11 localizes neither to the plasma membrane nor to the vacuole, but to a punctate endomembrane compartment that largely coincides with the distribution of the trans-Golgi marker sialyl transferase. Golgi-based manganese accumulation might therefore result in manganese tolerance through vesicular trafficking and exocytosis. In accord with this proposal, Arabidopsis mtp11 mutants exhibit enhanced manganese concentrations in shoots and roots. We propose that Golgi-mediated exocytosis comprises a conserved mechanism for heavy metal tolerance in plants.Golgi ͉ heavy metal transport ͉ metal tolerance protein ͉ metal trafficking ͉ manganese transporter T ransition metals are required by living systems where they perform a wide variety of functions as cofactors for enzymes and transcription factors. Transition metals are also present in many environments at potentially toxic concentrations, and this has led to the evolution of mechanisms that counter toxicity. In plants exposed to high concentrations of transition metals in the soil, binding of the metals to phytochelatins in the cytosol lowers metal activity (1). Additionally, metals can be removed from the cytosol through the action of metal transporters. Transporters involved in metal tolerance localize to the plasma membrane, thereby removing metals from the cell, or to the vacuolar membrane, where the metal can be sequestered into a large and metabolically relatively inert intracellular compartment (2).Manganese is the second most prevalent transition metal, after iron, in the Earth's crust and an essential micronutrient for all organisms, including humans and plants (3). In addition to being a cofactor for a variety of enzymes (including various decarboxylases of the tricarboxylic acid cycle, RNA polymerases, and numerous glyco...

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Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity

Cited by 372 publications

References 57 publications

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Demonstration and Characterization of the Heterodimerization of ZnT5 and ZnT6 in the Early Secretory Pathway

A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance

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