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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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Kinship of MIS mam-like genes with MAI mam genes of M. gryphiswaldense MSR-1.A) Partial sequence alignment of MamE proteins from the Magnetospirillum genus. B) Protein sequence alignment between MamQ-like encoded in the MIS of AMB-1, the newly identified MamQ-like from MSR-1 (MGR_0326) and MamQ encoded in the MAI of AMB-1.
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pone-0009151-g009: Kinship of MIS mam-like genes with MAI mam genes of M. gryphiswaldense MSR-1.A) Partial sequence alignment of MamE proteins from the Magnetospirillum genus. B) Protein sequence alignment between MamQ-like encoded in the MIS of AMB-1, the newly identified MamQ-like from MSR-1 (MGR_0326) and MamQ encoded in the MAI of AMB-1.

Mentions: In terms of reflecting protein evolution, phylogenetic trees based on protein sequence alignments are much more difficult to build and interpret than codon usage-based trees. Nevertheless both methods concur that sequences of MIS Mam-like proteins tend to cluster with protein sequences encoded in the MAI of Magnetospirilla, and are very distant from MC-1 Mam protein sequences (data not shown). Only inspection of protein alignments “by eye” yielded useful information from which to infer phylogenetic relationships in the Magnetospirillum sub-tree, as illustrated by MamE-like. The predicted MamE-like protein is more similar to MAI MamE of MSR-1 (56.3% identity) than the equivalent in AMB-1 (51.2% identity). Furthermore, there is a stretch of 50 residues in MamE-like (from Asn434 to Gln484) which is absent in MamE of AMB-1 and MS-1, but present in MamE of MSR-1 with 68.6% identity (Fig. 9A). MamQ-like is also very similar to MGR_0326 (63.5% identity, Fig. 8B), an MSR-1 protein whose similarity with MamQ has not been reported before; the identity between MamQ-like and MamQ in AMB-1 is only 37.5% (Fig. 9B). We searched for a genomic islet in the vicinity of MGR_0326 but could not find any additional Mam-like proteins in the M. gryphiswaldense MSR-1 genome. MGR_0326 is close to the mreBCD gene cluster (MGR_3222 to MGR_3224) involved in rod-shape determination. Naturally such a cluster exists in M. magneticum AMB-1 (amb3513 to amb3515) but no nearby MamQ-like protein could be found. For MamK, examination of sequence alignments of proteins belonging to the Magnetospirillum genus reveals that MamK-like is more closely related to the MSR-1 protein (see positions 40, 83, 118 and 257 in MSR-1, see Fig. 3A). When taken together these analyses suggest that Mam-like proteins encoded in the MIS evolved in a similar fashion to those encoded within the MAI of MSR-1, rather than of AMB-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)

Kinship of MIS mam-like genes with MAI mam genes of M. gryphiswaldense MSR-1.A) Partial sequence alignment of MamE proteins from the Magnetospirillum genus. B) Protein sequence alignment between MamQ-like encoded in the MIS of AMB-1, the newly identified MamQ-like from MSR-1 (MGR_0326) and MamQ encoded in the MAI of AMB-1.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009151-g009: Kinship of MIS mam-like genes with MAI mam genes of M. gryphiswaldense MSR-1.A) Partial sequence alignment of MamE proteins from the Magnetospirillum genus. B) Protein sequence alignment between MamQ-like encoded in the MIS of AMB-1, the newly identified MamQ-like from MSR-1 (MGR_0326) and MamQ encoded in the MAI of AMB-1.
Mentions: In terms of reflecting protein evolution, phylogenetic trees based on protein sequence alignments are much more difficult to build and interpret than codon usage-based trees. Nevertheless both methods concur that sequences of MIS Mam-like proteins tend to cluster with protein sequences encoded in the MAI of Magnetospirilla, and are very distant from MC-1 Mam protein sequences (data not shown). Only inspection of protein alignments “by eye” yielded useful information from which to infer phylogenetic relationships in the Magnetospirillum sub-tree, as illustrated by MamE-like. The predicted MamE-like protein is more similar to MAI MamE of MSR-1 (56.3% identity) than the equivalent in AMB-1 (51.2% identity). Furthermore, there is a stretch of 50 residues in MamE-like (from Asn434 to Gln484) which is absent in MamE of AMB-1 and MS-1, but present in MamE of MSR-1 with 68.6% identity (Fig. 9A). MamQ-like is also very similar to MGR_0326 (63.5% identity, Fig. 8B), an MSR-1 protein whose similarity with MamQ has not been reported before; the identity between MamQ-like and MamQ in AMB-1 is only 37.5% (Fig. 9B). We searched for a genomic islet in the vicinity of MGR_0326 but could not find any additional Mam-like proteins in the M. gryphiswaldense MSR-1 genome. MGR_0326 is close to the mreBCD gene cluster (MGR_3222 to MGR_3224) involved in rod-shape determination. Naturally such a cluster exists in M. magneticum AMB-1 (amb3513 to amb3515) but no nearby MamQ-like protein could be found. For MamK, examination of sequence alignments of proteins belonging to the Magnetospirillum genus reveals that MamK-like is more closely related to the MSR-1 protein (see positions 40, 83, 118 and 257 in MSR-1, see Fig. 3A). When taken together these analyses suggest that Mam-like proteins encoded in the MIS evolved in a similar fashion to those encoded within the MAI of MSR-1, rather than of AMB-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