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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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General codon usage analysis.RSCU-based trees generated with the Fitch-Margoliash distance-based optimization method. The best trees were computed by the algorithm from 100 randomized input order distance matrixes. A) mamD gene family. B) mamE gene family. C) mamK gene families. MamE-II (for MS-1 and AMB-1) are MamE homologues encoded in the MAI. Sub-trees comprising mam-like genes from the AMB-1 magnetotaxis islet are shaded grey. Boxed gene names are the mam genes belonging to the AMB-1 magnetosome island. Accession numbers for the encoded proteins are listed in Table S1.
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pone-0009151-g008: General codon usage analysis.RSCU-based trees generated with the Fitch-Margoliash distance-based optimization method. The best trees were computed by the algorithm from 100 randomized input order distance matrixes. A) mamD gene family. B) mamE gene family. C) mamK gene families. MamE-II (for MS-1 and AMB-1) are MamE homologues encoded in the MAI. Sub-trees comprising mam-like genes from the AMB-1 magnetotaxis islet are shaded grey. Boxed gene names are the mam genes belonging to the AMB-1 magnetosome island. Accession numbers for the encoded proteins are listed in Table S1.

Mentions: Tracing back the origin of this MIS is no simple matter. Most of the genes encoded are MTB-specific and as a consequence there is a very limited number of homologous genes and proteins to work with (11 sequences for mamK but only 4 sequences for mamJ which to date has only been found in Magnetospirilla). The significant difference in GC content prompted us to examine the codon usage pattern in the MIS and compare it with those of other known mam or mam-like genes. We generated phylogenetic trees allowing us to group these genes based on codon usage, at least for the 5 mam-like genes universally shared by MTBs, i.e. mamE-, mamK-, mamQ-, mamD- and mamF-like (only Desulfovibrio magneticus RS-1 is devoid of MamD). Although statistical bias may be introduced using only short sequences (mamF-like for instance with only 112 codons) there was good accordance between all trees thus constructed. Fig. 8 shows the codon usage-based phylogenetic trees built for mamD-, mamE- and mamK-like (for the 4 remaining mam-like genes, data not shown). Without exception mam-like genes group together with Magnetococcus sp. MC-1 homologues, as well as in most cases with those from marine magnetotactic vibrio strain MV-1 (shaded boxes in Fig. 8). MAI genes from Magnetospirilla are grouped together. This result clearly establishes the common origin of the genetic material from which MAIs from MC-1 and MV-1 and the MIS from AMB-1 evolved.


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)

General codon usage analysis.RSCU-based trees generated with the Fitch-Margoliash distance-based optimization method. The best trees were computed by the algorithm from 100 randomized input order distance matrixes. A) mamD gene family. B) mamE gene family. C) mamK gene families. MamE-II (for MS-1 and AMB-1) are MamE homologues encoded in the MAI. Sub-trees comprising mam-like genes from the AMB-1 magnetotaxis islet are shaded grey. Boxed gene names are the mam genes belonging to the AMB-1 magnetosome island. Accession numbers for the encoded proteins are listed in Table S1.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009151-g008: General codon usage analysis.RSCU-based trees generated with the Fitch-Margoliash distance-based optimization method. The best trees were computed by the algorithm from 100 randomized input order distance matrixes. A) mamD gene family. B) mamE gene family. C) mamK gene families. MamE-II (for MS-1 and AMB-1) are MamE homologues encoded in the MAI. Sub-trees comprising mam-like genes from the AMB-1 magnetotaxis islet are shaded grey. Boxed gene names are the mam genes belonging to the AMB-1 magnetosome island. Accession numbers for the encoded proteins are listed in Table S1.
Mentions: Tracing back the origin of this MIS is no simple matter. Most of the genes encoded are MTB-specific and as a consequence there is a very limited number of homologous genes and proteins to work with (11 sequences for mamK but only 4 sequences for mamJ which to date has only been found in Magnetospirilla). The significant difference in GC content prompted us to examine the codon usage pattern in the MIS and compare it with those of other known mam or mam-like genes. We generated phylogenetic trees allowing us to group these genes based on codon usage, at least for the 5 mam-like genes universally shared by MTBs, i.e. mamE-, mamK-, mamQ-, mamD- and mamF-like (only Desulfovibrio magneticus RS-1 is devoid of MamD). Although statistical bias may be introduced using only short sequences (mamF-like for instance with only 112 codons) there was good accordance between all trees thus constructed. Fig. 8 shows the codon usage-based phylogenetic trees built for mamD-, mamE- and mamK-like (for the 4 remaining mam-like genes, data not shown). Without exception mam-like genes group together with Magnetococcus sp. MC-1 homologues, as well as in most cases with those from marine magnetotactic vibrio strain MV-1 (shaded boxes in Fig. 8). MAI genes from Magnetospirilla are grouped together. This result clearly establishes the common origin of the genetic material from which MAIs from MC-1 and MV-1 and the MIS from AMB-1 evolved.

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