Vermamoeba vermiformis CDC-19 draft genome sequence reveals considerable gene trafficking including with candidate phyla radiation and giant viruses

Abstract

Vermamoeba vermiformis is a predominant free-living amoeba in human environments and amongst the most common amoebae that can cause severe infections in humans. it is a niche for numerous amoeba-resisting microorganisms such as bacteria and giant viruses. Differences in the susceptibility to these giant viruses have been observed. V. vermiformis and amoeba-resisting microorganisms share a sympatric lifestyle that can promote exchanges of genetic material. This work analyzed the first draft genome sequence of a V. vermiformis strain (CDC-19) through comparative genomic, transcriptomic and phylogenetic analyses. the genome of V. vermiformis is 59.5 megabase pairs in size, and 22,483 genes were predicted. A high proportion (10% (n = 2,295)) of putative genes encoded proteins showed the highest sequence homology with a bacterial sequence. the expression of these genes was demonstrated for some bacterial homologous genes. In addition, for 30 genes, we detected best BLAST hits with members of the Candidate Phyla Radiation. Moreover, 185 genes (0.8%) best matched with giant viruses, mostly those related to the subfamily Klosneuvirinae (101 genes), in particular Bodo saltans virus (69 genes). Lateral sequence transfers between V. vermiformis and amoeba-resisting microorganisms were strengthened by Sanger sequencing, transcriptomic and phylogenetic analyses. This work provides important insights and genetic data for further studies about this amoeba and its interactions with microorganisms. Amoebozoa species are widely distributed in different environments from terrestrial to aquatic ecosystems, where they can play important ecological roles 1,2. Members of the family Hartmannellidae are frequently detected along with a few other amoebae belonging to different genera of the taxon Amoebozoa 3. Vermamoeba vermiformis, a free-living amoeba of the family Hartmannellidae, formerly named Hartmannella vermiformis, was first isolated in freshwater from the Pigeon Lake, Wisconsin, and the Kankakee River, Indiana (United States) 4. V. vermiformis was thereafter commonly found in fresh surface water 5 , and also in tap water, bottled mineral water, thermal water, and recreational water environments such as fountains and swimming pools 6-8. Its density in drinking water sources and biofilms is higher than that of Acanthamoeba castellanii 9. V. vermiformis has two-stage life, switching between trophozoite and cystic form 3. Free-living amoebae (FLA) are commonly in contact with animals including humans. V. vermiformis was found to be the predominant amoeba in human environments 10,11 , and has been isolated more frequently from different hospital water systems than Acanthamoeba spp. 12. This amoeba is of special interest for human health as it is able, along with other Amoebozoa members including Acanthamoeba spp., to cause severe infections such as human keratitis 13-15. Despite its prevalence in human environments and its pathogenicity in humans, the genome of V. vermiformis had not been sequenced.

Simultaneous hybrid genome sequencing of Vermamoeba vermiformis and its Dependentiae endosymbiont Vermiphilus pyriformis

“…The sequencing of Vermamoeba vermiformis genome yielded 149 contigs, representing a total size of 39.5 Mb with an estimated completeness of 88.7% (Table 1). The genome size considerably differs from a previously published genome of another V. vermiformis strain (59.5 Mb), though GC content is comparable (14). Among contigs attributed to V. vermiformis, one stood out by its high coverage and low GC content, as compared with other V. vermiformis contigs.…”

Rhizomal Reclassification of Living Organisms

“…Moreover, several studies suggest that eukaryotic nuclei are originated from an ancient NCLDV [ 56 ]. Finally, with the recent demonstration of the integration of many giant virus genes inside amoebae [ 68 , 69 ], the mosaicism of eukaryotes appears to involve several bacteria, archaea, and other organisms [ 70 ]. The genome of a eukaryote (amoeba, plants, etc.)…”

“…This lifestyle leads to the coexistence of several parasites and/or symbionts in the same amoeba. Subsequently, the giant virus is exposed to a group of multisource genes [ 69 , 78 ]. This type of interaction likely produces organisms with highly mosaic and chimeric genomes, such as giant viruses [ 43 , 78 ].…”

Adapted protocol for Saccharibacteria co-cultivation: two new members join the club of Candidate Phyla radiation

“…Concerning their origin, the presence of archaeal/eukaryotic sequences suggests the presence of an interaction between these microorganisms in their shared niche (4,30,31). The mosaic structure of CPR in general gives them a unique characteristic, comparable to one another and different from other microbial domains (4).…”