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Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae.

Pagnier I, Yutin N, Croce O, Makarova KS, Wolf YI, Benamar S, Raoult D, Koonin EV, La Scola B - Biol. Direct (2015)

Bottom Line: This unique mechanism of cell division is associated with a deep degradation of the cell division machinery and delayed expression of the ftsZ gene.Horizontal gene transfer is likely to be facilitated by the cohabitation of diverse parasites and symbionts inside amoeba.This article was reviewed by Dr. Igor Zhulin, Dr. Jeremy Selengut, and Pr Martijn Huynen.

View Article: PubMed Central - PubMed

Affiliation: URMITE, CNRS UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Bd. Jean Moulin, 13385, Marseille Cedex 5, France. isabelle.pagnier@univ-amu.fr.

ABSTRACT

Background: Only a small fraction of bacteria and archaea that are identifiable by metagenomics can be grown on standard media. Recent efforts on deep metagenomics sequencing, single-cell genomics and the use of specialized culture conditions (culturomics) increasingly yield novel microbes some of which represent previously uncharacterized phyla and possess unusual biological traits.

Results: We report isolation and genome analysis of Babela massiliensis, an obligate intracellular parasite of Acanthamoeba castellanii. B. massiliensis shows an unusual, fission mode of cell multiplication whereby large, polymorphic bodies accumulate in the cytoplasm of infected amoeba and then split into mature bacterial cells. This unique mechanism of cell division is associated with a deep degradation of the cell division machinery and delayed expression of the ftsZ gene. The genome of B. massiliensis consists of a circular chromosome approximately 1.12 megabase in size that encodes, 981 predicted proteins, 38 tRNAs and one typical rRNA operon. Phylogenetic analysis shows that B. massiliensis belongs to the putative bacterial phylum TM6 that so far was represented by the draft genome of the JCVI TM6SC1 bacterium obtained by single cell genomics and numerous environmental sequences.

Conclusions: Currently, B. massiliensis is the only cultivated member of the putative TM6 phylum. Phylogenomic analysis shows diverse taxonomic affinities for B. massiliensis genes, suggestive of multiple gene acquisitions via horizontal transfer from other bacteria and eukaryotes. Horizontal gene transfer is likely to be facilitated by the cohabitation of diverse parasites and symbionts inside amoeba. B. massiliensis encompasses many genes encoding proteins implicated in parasite-host interaction including the greatest number of ankyrin repeats among sequenced bacteria and diverse proteins related to the ubiquitin system. Characterization of B. massiliensis, a representative of a distinct bacterial phylum, thanks to its ability to grow in amoeba, reaffirms the critical role of diverse culture approaches in microbiology.

Reviewers: This article was reviewed by Dr. Igor Zhulin, Dr. Jeremy Selengut, and Pr Martijn Huynen.

No MeSH data available.


Circular representation of theBabela massiliensischromosome. Circles from the center to the outside: GC skew (green/purple), GC content (black), tRNA (blue) and rRNA (green) on forward strand, ankyrins (red arrows) on forward strand, genes on forward strand colored by COGs categories, genes on reverse strand colored by COGs categories, ankyrins (red arrows) on reverse strand.
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Fig2: Circular representation of theBabela massiliensischromosome. Circles from the center to the outside: GC skew (green/purple), GC content (black), tRNA (blue) and rRNA (green) on forward strand, ankyrins (red arrows) on forward strand, genes on forward strand colored by COGs categories, genes on reverse strand colored by COGs categories, ankyrins (red arrows) on reverse strand.

Mentions: The genome of B. massiliensis consists of a single circular chromosome with the size of 1,118,422 bp and a GC content of 27.4%. In total, 981 protein-coding sequences (CDS) were identified, with 198 (~20%) of the predicted proteins showing no detectable sequence similarity to other proteins in public databases (including those of JCVI TM6SC1) (Figure 2). Notably, the B. massiliensis genome encompasses a relatively large number of tandem gene duplications (37, compared to 17 in TM6SC1). The CDS annotation shows a relatively low coverage with Clusters of Orthologous Genes (COGs) (652 genes, i.e. 66% of the CDS, compared to the average of approximately 75% for a representative genome set) [18]. The genome encodes one typical rRNA operon, 38 tRNAs (for all amino acids), 4.8S (Signal Recognition Particle) RNA, tmRNA and the RNA component of RNAse P. No phage or plasmid- related genes were identified, and only one IS4 family transposase gene was detected. This observation is in a sharp contrast to the high proportion (24% of the protein-coding genes) of predicted mobile genetic elements in the genome of “Ca. Amoebophilus asiaticus”, another intracellular parasite of amoeba [19]. As expected of an obligate intracellular symbiont, B. massiliensis encodes only 5 predicted transcription regulators. A single putative replication origin was predicted at 152 nt upstream of the start of the dnaA gene using GCskew analysis.Figure 2


Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae.

Pagnier I, Yutin N, Croce O, Makarova KS, Wolf YI, Benamar S, Raoult D, Koonin EV, La Scola B - Biol. Direct (2015)

Circular representation of theBabela massiliensischromosome. Circles from the center to the outside: GC skew (green/purple), GC content (black), tRNA (blue) and rRNA (green) on forward strand, ankyrins (red arrows) on forward strand, genes on forward strand colored by COGs categories, genes on reverse strand colored by COGs categories, ankyrins (red arrows) on reverse strand.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4378268&req=5

Fig2: Circular representation of theBabela massiliensischromosome. Circles from the center to the outside: GC skew (green/purple), GC content (black), tRNA (blue) and rRNA (green) on forward strand, ankyrins (red arrows) on forward strand, genes on forward strand colored by COGs categories, genes on reverse strand colored by COGs categories, ankyrins (red arrows) on reverse strand.
Mentions: The genome of B. massiliensis consists of a single circular chromosome with the size of 1,118,422 bp and a GC content of 27.4%. In total, 981 protein-coding sequences (CDS) were identified, with 198 (~20%) of the predicted proteins showing no detectable sequence similarity to other proteins in public databases (including those of JCVI TM6SC1) (Figure 2). Notably, the B. massiliensis genome encompasses a relatively large number of tandem gene duplications (37, compared to 17 in TM6SC1). The CDS annotation shows a relatively low coverage with Clusters of Orthologous Genes (COGs) (652 genes, i.e. 66% of the CDS, compared to the average of approximately 75% for a representative genome set) [18]. The genome encodes one typical rRNA operon, 38 tRNAs (for all amino acids), 4.8S (Signal Recognition Particle) RNA, tmRNA and the RNA component of RNAse P. No phage or plasmid- related genes were identified, and only one IS4 family transposase gene was detected. This observation is in a sharp contrast to the high proportion (24% of the protein-coding genes) of predicted mobile genetic elements in the genome of “Ca. Amoebophilus asiaticus”, another intracellular parasite of amoeba [19]. As expected of an obligate intracellular symbiont, B. massiliensis encodes only 5 predicted transcription regulators. A single putative replication origin was predicted at 152 nt upstream of the start of the dnaA gene using GCskew analysis.Figure 2

Bottom Line: This unique mechanism of cell division is associated with a deep degradation of the cell division machinery and delayed expression of the ftsZ gene.Horizontal gene transfer is likely to be facilitated by the cohabitation of diverse parasites and symbionts inside amoeba.This article was reviewed by Dr. Igor Zhulin, Dr. Jeremy Selengut, and Pr Martijn Huynen.

View Article: PubMed Central - PubMed

Affiliation: URMITE, CNRS UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Bd. Jean Moulin, 13385, Marseille Cedex 5, France. isabelle.pagnier@univ-amu.fr.

ABSTRACT

Background: Only a small fraction of bacteria and archaea that are identifiable by metagenomics can be grown on standard media. Recent efforts on deep metagenomics sequencing, single-cell genomics and the use of specialized culture conditions (culturomics) increasingly yield novel microbes some of which represent previously uncharacterized phyla and possess unusual biological traits.

Results: We report isolation and genome analysis of Babela massiliensis, an obligate intracellular parasite of Acanthamoeba castellanii. B. massiliensis shows an unusual, fission mode of cell multiplication whereby large, polymorphic bodies accumulate in the cytoplasm of infected amoeba and then split into mature bacterial cells. This unique mechanism of cell division is associated with a deep degradation of the cell division machinery and delayed expression of the ftsZ gene. The genome of B. massiliensis consists of a circular chromosome approximately 1.12 megabase in size that encodes, 981 predicted proteins, 38 tRNAs and one typical rRNA operon. Phylogenetic analysis shows that B. massiliensis belongs to the putative bacterial phylum TM6 that so far was represented by the draft genome of the JCVI TM6SC1 bacterium obtained by single cell genomics and numerous environmental sequences.

Conclusions: Currently, B. massiliensis is the only cultivated member of the putative TM6 phylum. Phylogenomic analysis shows diverse taxonomic affinities for B. massiliensis genes, suggestive of multiple gene acquisitions via horizontal transfer from other bacteria and eukaryotes. Horizontal gene transfer is likely to be facilitated by the cohabitation of diverse parasites and symbionts inside amoeba. B. massiliensis encompasses many genes encoding proteins implicated in parasite-host interaction including the greatest number of ankyrin repeats among sequenced bacteria and diverse proteins related to the ubiquitin system. Characterization of B. massiliensis, a representative of a distinct bacterial phylum, thanks to its ability to grow in amoeba, reaffirms the critical role of diverse culture approaches in microbiology.

Reviewers: This article was reviewed by Dr. Igor Zhulin, Dr. Jeremy Selengut, and Pr Martijn Huynen.

No MeSH data available.