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. 2018 Jul 17:14:1176934318788337.
doi: 10.1177/1176934318788337. eCollection 2018.

Lateral Gene Transfer Between Protozoa-Related Giant Viruses of Family Mimiviridae and Chlamydiae

Takanori Watanabe  1 , Sumire Yamazaki  1 , Chinatsu Maita  1 , Mizue Matushita  1 , Junji Matsuo  1 , Torahiko Okubo  1 , Hiroyuki Yamaguchi  1
Affiliations

Lateral Gene Transfer Between Protozoa-Related Giant Viruses of Family Mimiviridae and Chlamydiae

Takanori Watanabe et al. Evol Bioinform Online. .

Abstract

Obligate intracellular chlamydiae diverged into pathogenic and environmental chlamydiae 0.7-1.4 billion years ago. While pathogenic chlamydiae have adapted to a wide range of vertebrates, environmental chlamydiae inhabit unicellular amoebae, the free-living Acanthamoeba. However, how and why this divergence occurred remains unclear. Meanwhile, giant viruses consisting of protozoa-related and protozoa-unrelated viruses have been discovered, with the former group being suggested to have more influenced environmental chlamydiae during their evolution while cohabiting host amoebae. Against this background, we attempted to visualize genes of giant viruses in chlamydial genomes by bioinformatic analysis mainly with comparative genome and phylogenic analysis, seeking genes present in chlamydiae that are specifically shared with protozoa-related giant viruses. As a result, in contrast to protozoa-unrelated giant viruses, the genes of protozoa-related giant viruses were significantly shared in both the chlamydia genomes depending on the giant virus type. In particular, the prevalence of Mimiviridae genes among the protozoa-related giant virus genes in chlamydial genomes was significantly high. Meanwhile, the prevalence of protozoa-related giant virus genes in pathogenic chlamydia genomes was consistently higher than those of environmental chlamydiae; the actual number of sequences similar to giant virus was also significantly predominant compared with those in the environmental chlamydial genomes. Among them, the most prevalent of giant virus was in the case of chlamydiae with Megavirus chiliensis; total of 1338 genes of the chlamydiae were found to be shared with the virus (444 genes specific to environmental chlamydiae, 892 genes shared between both chlamydiae, only two genes in the pathogenic chlamydiae). Phylogenic analysis with most prevalent sets (Megavirus chiliensis and Protochlamydia EI2 or Chlamydia trachomatis L2 434Bu) showed the presence of orthologs between these with several clustered. In addition, Pearson's single regression analysis revealed that almost the prevalence of the genes from the giant viruses in chlamydial genomes was negatively and specifically correlated with the number of chlamydial open reading frames (ORFs). Thus, these results indicated the trace of lateral gene transfer between protozoa-related giant viruses of family Mimiviridae and chlamydiae. This is the first demonstration of a putative linkage between chlamydiae and the giant viruses, providing us with a hint to understand chlamydial evolution.

Keywords: Acanthamoeba; Giant virus; Mimiviridae; environmental chlamydiae; evolution; pathogenic chlamydiae.

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Conflict of interest statement

Declaration of Conflicting Interests:The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Figures

Figure 1.
Figure 1.
Comparisons of the prevalence rates of giant virus genes in chlamydial genomes and of the trend of dispersion on the prevalence of giant virus genes between pathogenic and environmental chlamydiae. Panels (A) and (B) show protozoa-related giant viruses and protozoa-unrelated giant viruses, respectively. Blue and red bars show the prevalence of giant virus genes in environmental and pathogenic chlamydial genomes, respectively. Comparisons of the prevalence rate were conducted using Mann–Whitney’s U test. Stars show a significant difference (P < .05) between the prevalence values of environmental and pathogenic chlamydiae. Green circles show a significant difference in the prevalence rate of giant virus genes with values more than cut-off. Cut-off (1.48%) as a background value (dashed line) was defined by the prevalence of genes from Mimiviridae (Cafeteria roenbergensis virus, Megavirus chilensis, Megavirus lba, Mimivirus, Moumouvirus) in the Escherichia coli K12 genome (1.28 ± 0.19%) (see Table S5).
Figure 2.
Figure 2.
Phylogenic analysis with most prevalent sets (Megavirus chiliensis and Protochlamydia EI2 or Chlamydia trachomatis L2 434Bu) showing several clusters. Trees (A) and (B) show Megavirus chiliensis (MegaVirus) with Protochlamydia EI2 (Proto_EI2) and with Chlamydia trachomatis L2 434Bu (Chlt_L2), respectively. Additional numbers (peg) show gene ID numbers assigned by RAST (see Table S1 to S4b). Black circles show these chlamydial genes. Phylogenic trees were constructed with a maximum parsimony method by using MAFFT version 7 (https://mafft.cbrc.jp/alignment/software/).
Figure 3.
Figure 3.
Total number of functional genes in each of the chlamydial genomes shared among protozoa-related giant viruses in the Mimiviridae (Megavirus chilensis). The genes shared between protozoa-related giant viruses in the Mimiviridae (Megavirus chilensis) and each of the chlamydiae were extracted, from a comparative genome analysis with RAST (see filter conditions into Material and Methods). Functional annotation was performed using the Kyoto Encyclopedia of Genes and Genomes (KEGG) or the Universal Protein Resource (UniProt). Upper panel: specific to environmental chlamydiae; Middle panel: shared between both chlamydiae; Lower panel: specific to pathogenic chlamydiae. Colors show distinct gene functions annotated by KEGG or UniProt. Pie charts in the center show the prevalence of genes classified into the categories of “Metabolic process,” “Regulation/modification,” “Structure,” and “Others.”
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