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Abstract
BackgroundOnly 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.ResultsWe 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.ConclusionsCurrently, 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.ReviewersThis article was reviewed by Dr. Igor Zhulin, Dr. Jeremy Selengut, and Pr Martijn Huynen.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-015-0043-z) contains supplementary material, which is available to authorized users.
Highlights
A small fraction of bacteria and archaea that are identifiable by metagenomics can be grown on standard media
We show that B. massiliensis is the only cultured bacterium from the putative TM6 phylum, for which only one, 90% complete genome, JCVI TM6SC1, has been reported through single cell genomics [13], but that apparently is extremely widespread in diverse habitats
Among the temperatures tested for growth in amoebal coculture, B. massiliensis was unable to grow at 4°C and 12°C but showed growth at 28°C and 37°C
Summary
A small fraction of bacteria and archaea that are identifiable by metagenomics can be grown on standard media. Since the onset of the genome sequencing era, evolution of obligate intracellular bacteria has been viewed in a sharp contrast to the evolution of free-living bacteria, especially those that inhabit complex environments Intracellular bacteria, such as Chlamydiae or Rickettsiae, were generally regarded as organisms characterized by extreme adaptation to a narrow ecological niche (the host cell) associated with a massive gene loss resulting in dramatic genome reduction [1,2,3]. In amoebae, intracellular bacteria are not genetically isolated but rather coexist sympatrically with other bacteria, archaea and NCLDV (Nucleocytoplasmic large DNA viruses), amoeba-associated giant viruses, a lifestyle that is conducive to HGT [10,11,12] Thanks to their capacity to engulf any large particle and to bring into proximity numerous, diverse microbes, amoebae appear to be a melting pot of evolution from which new genes, new associations of genes and new life forms have been emerging throughout the course of evolution [12]
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