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A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome island.

Rioux JB, Philippe N, Pereira S, Pignol D, Wu LF, Ginet N - PLoS ONE (2010)

Bottom Line: In addition, we demonstrate that mamK-like is transcribed in AMB-1 wild-type and DeltamamK mutant cells and that the actin-like filamentous structures observed in the DeltamamK strain are probably MamK-like polymers.Thus MamK-like is a new member of the prokaryotic actin-like family.This is the first evidence of a functional mam gene encoded outside the magnetosome genomic island.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Bioénergétique Cellulaire - Institut de Biologie Environnementale et Biotechnologie, Commissariat à l'Energie Atomique, Saint-Paul-lez-Durance, France.

ABSTRACT
Magnetotactic bacteria are able to swim navigating along geomagnetic field lines. They synthesize ferromagnetic nanocrystals that are embedded in cytoplasmic membrane invaginations forming magnetosomes. Regularly aligned in the cytoplasm along cytoskeleton filaments, the magnetosome chain effectively forms a compass needle bestowing on bacteria their magnetotactic behaviour. A large genomic island, conserved among magnetotactic bacteria, contains the genes potentially involved in magnetosome formation. One of the genes, mamK has been described as encoding a prokaryotic actin-like protein which when it polymerizes forms in the cytoplasm filamentous structures that provide the scaffold for magnetosome alignment. Here, we have identified a series of genes highly similar to the mam genes in the genome of Magnetospirillum magneticum AMB-1. The newly annotated genes are clustered in a genomic islet distinct and distant from the known magnetosome genomic island and most probably acquired by lateral gene transfer rather than duplication. We focused on a mamK-like gene whose product shares 54.5% identity with the actin-like MamK. Filament bundles of polymerized MamK-like protein were observed in vitro with electron microscopy and in vivo in E. coli cells expressing MamK-like-Venus fusions by fluorescence microscopy. In addition, we demonstrate that mamK-like is transcribed in AMB-1 wild-type and DeltamamK mutant cells and that the actin-like filamentous structures observed in the DeltamamK strain are probably MamK-like polymers. Thus MamK-like is a new member of the prokaryotic actin-like family. This is the first evidence of a functional mam gene encoded outside the magnetosome genomic island.

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A magnetotaxis islet.Genetic organization of the magnetotaxis islet (MIS) compared to the magnetosome island (MAI) in M. magneticum AMB-1. Each mam gene in the MAI and its respective homologue in the MIS are shown in the same colour. Scale bars: 1 kb. A) The region including mam-like genes is situated between nucleotides (nt) 421600 and 450000 on the bacterial chromosome. For clarity ORFs unrelated to mam genes are not shown. B) Only the mamGFDC and mamAB operons from the MAI (nt 997403 to 1095895) are shown.
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pone-0009151-g001: A magnetotaxis islet.Genetic organization of the magnetotaxis islet (MIS) compared to the magnetosome island (MAI) in M. magneticum AMB-1. Each mam gene in the MAI and its respective homologue in the MIS are shown in the same colour. Scale bars: 1 kb. A) The region including mam-like genes is situated between nucleotides (nt) 421600 and 450000 on the bacterial chromosome. For clarity ORFs unrelated to mam genes are not shown. B) Only the mamGFDC and mamAB operons from the MAI (nt 997403 to 1095895) are shown.

Mentions: Among the seven ORFs, five are homologous to genes belonging to the mamAB operon (mamE, mamJ, mamK, mamL and mamQ) and the two remaining are similar to genes from the mamGFDC operon (mamF and mamD), both operons being located within the MAI. MamK and MamJ are involved in magnetosome alignment, MamE is a predicted serine protease (similar to DegP in E. coli and potentially involved in Fe2+-induced oxidative stress remediation [38]), and the molecular functions of MamL and MamQ are unknown. The hydrophobic MamD and MamF are found exclusively in the magnetosome membrane; they are involved in regulating magnetite crystal size though the underlying molecular mechanisms remain unknown [15]. The genetic organization of the mam-like genes differs from their MAI counterparts since the seven mam-like genes are scattered over a region of about 22 kb (Fig. 1).


A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome island.

Rioux JB, Philippe N, Pereira S, Pignol D, Wu LF, Ginet N - PLoS ONE (2010)

A magnetotaxis islet.Genetic organization of the magnetotaxis islet (MIS) compared to the magnetosome island (MAI) in M. magneticum AMB-1. Each mam gene in the MAI and its respective homologue in the MIS are shown in the same colour. Scale bars: 1 kb. A) The region including mam-like genes is situated between nucleotides (nt) 421600 and 450000 on the bacterial chromosome. For clarity ORFs unrelated to mam genes are not shown. B) Only the mamGFDC and mamAB operons from the MAI (nt 997403 to 1095895) are shown.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2818848&req=5

pone-0009151-g001: A magnetotaxis islet.Genetic organization of the magnetotaxis islet (MIS) compared to the magnetosome island (MAI) in M. magneticum AMB-1. Each mam gene in the MAI and its respective homologue in the MIS are shown in the same colour. Scale bars: 1 kb. A) The region including mam-like genes is situated between nucleotides (nt) 421600 and 450000 on the bacterial chromosome. For clarity ORFs unrelated to mam genes are not shown. B) Only the mamGFDC and mamAB operons from the MAI (nt 997403 to 1095895) are shown.
Mentions: Among the seven ORFs, five are homologous to genes belonging to the mamAB operon (mamE, mamJ, mamK, mamL and mamQ) and the two remaining are similar to genes from the mamGFDC operon (mamF and mamD), both operons being located within the MAI. MamK and MamJ are involved in magnetosome alignment, MamE is a predicted serine protease (similar to DegP in E. coli and potentially involved in Fe2+-induced oxidative stress remediation [38]), and the molecular functions of MamL and MamQ are unknown. The hydrophobic MamD and MamF are found exclusively in the magnetosome membrane; they are involved in regulating magnetite crystal size though the underlying molecular mechanisms remain unknown [15]. The genetic organization of the mam-like genes differs from their MAI counterparts since the seven mam-like genes are scattered over a region of about 22 kb (Fig. 1).

Bottom Line: In addition, we demonstrate that mamK-like is transcribed in AMB-1 wild-type and DeltamamK mutant cells and that the actin-like filamentous structures observed in the DeltamamK strain are probably MamK-like polymers.Thus MamK-like is a new member of the prokaryotic actin-like family.This is the first evidence of a functional mam gene encoded outside the magnetosome genomic island.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Bioénergétique Cellulaire - Institut de Biologie Environnementale et Biotechnologie, Commissariat à l'Energie Atomique, Saint-Paul-lez-Durance, France.

ABSTRACT
Magnetotactic bacteria are able to swim navigating along geomagnetic field lines. They synthesize ferromagnetic nanocrystals that are embedded in cytoplasmic membrane invaginations forming magnetosomes. Regularly aligned in the cytoplasm along cytoskeleton filaments, the magnetosome chain effectively forms a compass needle bestowing on bacteria their magnetotactic behaviour. A large genomic island, conserved among magnetotactic bacteria, contains the genes potentially involved in magnetosome formation. One of the genes, mamK has been described as encoding a prokaryotic actin-like protein which when it polymerizes forms in the cytoplasm filamentous structures that provide the scaffold for magnetosome alignment. Here, we have identified a series of genes highly similar to the mam genes in the genome of Magnetospirillum magneticum AMB-1. The newly annotated genes are clustered in a genomic islet distinct and distant from the known magnetosome genomic island and most probably acquired by lateral gene transfer rather than duplication. We focused on a mamK-like gene whose product shares 54.5% identity with the actin-like MamK. Filament bundles of polymerized MamK-like protein were observed in vitro with electron microscopy and in vivo in E. coli cells expressing MamK-like-Venus fusions by fluorescence microscopy. In addition, we demonstrate that mamK-like is transcribed in AMB-1 wild-type and DeltamamK mutant cells and that the actin-like filamentous structures observed in the DeltamamK strain are probably MamK-like polymers. Thus MamK-like is a new member of the prokaryotic actin-like family. This is the first evidence of a functional mam gene encoded outside the magnetosome genomic island.

Show MeSH
Related in: MedlinePlus