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. 2018 Sep 6:9:2098.
doi: 10.3389/fmicb.2018.02098. eCollection 2018.

A Phylogenomic Study of Acanthamoeba polyphaga Draft Genome Sequences Suggests Genetic Exchanges With Giant Viruses

Nisrine Chelkha  1 , Anthony Levasseur  1 , Pierre Pontarotti  1 , Didier Raoult  1 , Bernard La Scola  1 , Philippe Colson  1
Affiliations

A Phylogenomic Study of Acanthamoeba polyphaga Draft Genome Sequences Suggests Genetic Exchanges With Giant Viruses

Nisrine Chelkha et al. Front Microbiol. .

Abstract

Acanthamoeba are ubiquitous phagocytes predominant in soil and water which can ingest many microbes. Giant viruses of amoebae are listed among the Acanthamoeba-resisting microorganisms. Their sympatric lifestyle within amoebae is suspected to promote lateral nucleotide sequence transfers. Some Acanthamoeba species have shown differences in their susceptibility to giant viruses. Until recently, only the genome of a single Acanthamoeba castellanii Neff was available. We analyzed the draft genome sequences of Acanthamoeba polyphaga through several approaches, including comparative genomics, phylogeny, and sequence networks, with the aim of detecting putative nucleotide sequence exchanges with giant viruses. We identified a putative sequence trafficking between this Acanthamoeba species and giant viruses, with 366 genes best matching with viral genes. Among viruses, Pandoraviruses provided the greatest number of best hits with 117 (32%) for A. polyphaga. Then, genes from mimiviruses, Mollivirus sibericum, marseilleviruses, and Pithovirus sibericum were best hits in 67 (18%), 35 (9%), 24 (7%), and 2 (0.5%) cases, respectively. Phylogenetic reconstructions showed in a few cases that the most parsimonious evolutionary scenarios were a transfer of gene sequences from giant viruses to A. polyphaga. Nevertheless, in most cases, phylogenies were inconclusive regarding the sense of the sequence flow. The number and nature of putative nucleotide sequence transfers between A. polyphaga, and A. castellanii ATCC 50370 on the one hand, and pandoraviruses, mimiviruses and marseilleviruses on the other hand were analyzed. The results showed a lower number of differences within the same giant viral family compared to between different giant virus families. The evolution of 10 scaffolds that were identified among the 14 Acanthamoeba sp. draft genome sequences and that harbored ≥ 3 genes best matching with viruses showed a conservation of these scaffolds and their 46 viral genes in A. polyphaga, A. castellanii ATCC 50370 and A. pearcei. In contrast, the number of conserved genes decreased for other Acanthamoeba species, and none of these 46 genes were present in three of them. Overall, this work opens up several potential avenues for future studies on the interactions between Acanthamoeba species and giant viruses.

Keywords: Acanthamoeba; Acanthamoeba polyphaga; draft genome sequences; giant viruses; horizontal gene transfer; mimivirus; nucleotide sequence transfer.

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Figures

FIGURE 1
FIGURE 1
Taxonomic distribution of the predicted proteins in A. polyphaga. (Left) All predicted proedicted proteins; (right) viral proteins. Other virus-like sequences than giant viruses are represented, encompassing the viral families or groups: Herpesviridae, Baculoviridae, Podoviridae, Nimaviridae, haloviruses, Dicistroviridae, Paramyxoviridae, Totiviridae, and Retroviridae, and Haloviruses.
FIGURE 2
FIGURE 2
Network of viral genes in A. polyphaga (A) and gene trafficking between A. polyphaga and giant viruses (B). (A) genes were classified regarding their viral families, and the number of exchanged genes was indicated for each group of viruses; (B) the 1,797 genes were classified with respect to their viral families, and represented by a different color: pandoraviruses in pink; mimiviruses in dark blue; marseilleviruses in light orange; light blue includes other amoeba viruses (Mollivirus sibericum and Pithovirus sibericum); and phycodnaviruses in green.
FIGURE 3
FIGURE 3
Phylogenetic trees for six examples of putative viral proteins in A. polyphaga. Gene sequence transfer was inferred from the comparison between annotated sequences with a putative viral origin and their best hits as well as their homologs in the other Acanthamoeba genomes. The way of the transfer was supposed to be from giant viruses to amoebae (a–c) or from amoebae to giant viruses (d–f). Trees are unrooted. In red: A. polyphaga gene; in blue: the viral homolog; in orange homologs from other Acanthamoeba species; in black: homologs from other organisms.
FIGURE 4
FIGURE 4
Rhizomes of A. polyphaga gene fragments illustrative of the mosaicism of the genes. Forty amino acid-long fragments of four A. polyphaga genes either supposed to have been transferred from viruses to amoebae (A,B) or in the opposite way (C,D) were linked to their most similar sequences in the NCBI GenBank protein sequence database according to the BLAST program (https://blast.ncbi.nlm.nih.gov/Blast.cgi), classified according to their belonging to viruses, eukaryotes, bacteria or archaea, and integrated in a circular gene data visualization. The figures were performed using the CIRCOS online tool (http://mkweb.bcgsc.ca/tableviewer/visualize/).
FIGURE 5
FIGURE 5
Comparison between gene synteny for genes with giant virus genes as best match in the genome sequence of 16 Acanthamoeba isolates classified in 14 species, and genome tree built for these Acanthamoeba species. Phylogenetic tree using the complete draft genome sequences of the 16 Acanthamoeba strains was represented aside the synteny distribution of genes best matching with giant virus genes in 10 selected genomic regions from Acanthamoeba spp. Phylogenetic reconstructions were performed using the alignment of 16 draft genome sequences of Acanthamoeba strains classified in 14 species including two A. polyphaga strains and two A. castellanii strains, by using the progressive Mauve program (Darling et al., 2010). Pointing triangles on the right part of the Figure correspond to viral genes; viruses are represented by different colors.
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References

    1. Abrahao J., Silva L., Santos Silva L., Bou Khalil J. Y., Rodrigues R., Arantes T., et al. (2018). Tailed giant tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9:749. 10.1038/s41467-018-03168-3161 - DOI - PMC - PubMed
    1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215 403–410. 10.1016/S0022-2836(05)80360-80362 - DOI - PubMed
    1. Antwerpen M. H., Georgi E., Zoeller L., Woelfel R., Stoecker K., Scheid P. (2015). Whole-genome sequencing of a Pandoravirus isolated from keratitis-inducing Acanthamoeba. Genome Announc. 3:e00136-15. 10.1128/genomeA.00136-15 - DOI - PMC - PubMed
    1. Bertelli C., Greub G. (2012). Lateral gene exchanges shape the genomes of amoeba-resisting microorganisms. Front. Cell. Infect. Microbiol. 2:110. 10.3389/fcimb.2012.00110 - DOI - PMC - PubMed
    1. Blanc G., Gallot-Lavallée L., Maumus F. (2015). Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses. Proc. Natl. Acad. Sci. U.S.A. 112 E5318–E5326. 10.1073/pnas.1506469112 - DOI - PMC - PubMed

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