title: Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae.
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.
authors.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.
authors.forename: Isabelle
authors.initials: I
authors.lastname: Pagnier
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA. yutin@ncbi.nlm.nih.gov.
authors.forename: Natalya
authors.initials: N
authors.lastname: Yutin
authors.affiliation: URMITE, CNRS UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Bd. Jean Moulin, 13385, Marseille Cedex 5, France. olivier.croce@gmail.com.
authors.forename: Olivier
authors.initials: O
authors.lastname: Croce
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA. makarova@ncbi.nlm.nih.gov.
authors.forename: Kira S
authors.initials: KS
authors.lastname: Makarova
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA. wolf@ncbi.nlm.nih.gov.
authors.forename: Yuri I
authors.initials: YI
authors.lastname: Wolf
authors.affiliation: URMITE, CNRS UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Bd. Jean Moulin, 13385, Marseille Cedex 5, France. benamarsamia@yahoo.fr.
authors.forename: Samia
authors.initials: S
authors.lastname: Benamar
authors.affiliation: URMITE, CNRS UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Bd. Jean Moulin, 13385, Marseille Cedex 5, France. didier.raoult@gmail.com.
authors.forename: Didier
authors.initials: D
authors.lastname: Raoult
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA. koonin@ncbi.nlm.nih.gov.
authors.forename: Eugene V
authors.initials: EV
authors.lastname: Koonin
authors.affiliation: URMITE, CNRS UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Bd. Jean Moulin, 13385, Marseille Cedex 5, France. bernard.la-scola@univ-amu.fr.
authors.forename: Bernard
authors.initials: B
authors.lastname: La Scola
mesh_terms: D048248:Acanthamoeba castellanii / Q000382:microbiology*; D001426:Bacterial Proteins / Q000235:genetics; D001483:Base Sequence; D018929:Cell Culture Techniques; D002455:Cell Division; D003470:Culture Media; D003593:Cytoplasm / Q000382:microbiology; D003598:Cytoskeletal Proteins / Q000235:genetics; D004269:DNA, Bacterial / Q000235:genetics; D020564:Deltaproteobacteria / Q000235:genetics* / Q000302:isolation & purification; D022761:Gene Transfer, Horizontal; D016680:Genome, Bacterial; D023281:Genomics; D008969:Molecular Sequence Data; D010802:Phylogeny; D012335:RNA, Ribosomal / Q000737:chemistry; D012343:RNA, Transfer / Q000737:chemistry; D017422:Sequence Analysis, DNA; D013559:Symbiosis
chemical_list: D001426:Bacterial Proteins; D003470:Culture Media; D003598:Cytoskeletal Proteins; D004269:DNA, Bacterial; C071525:FtsZ protein, Bacteria; D012335:RNA, Ribosomal; D012343:RNA, Transfer