Lamarckian evolution of the giant Mimivirus in allopatric laboratory culture on amoebae

Abstract

Acanthamoeba polyphaga Mimivirus has been subcultured 150 times on germ-free amoebae. This allopatric niche is very different from that found in the natural environment, where the virus is in competition with many other organisms. In this experiment, substantial gene variability and loss occurred concurrently with the emergence of phenotypically different viruses. We sought to quantify the respective roles of Lamarckian and Darwinian evolution during this experiment. We postulated that the Mimivirus genes that were down-regulated at the beginning of the allopatric laboratory culture and inactivated after 150 passages experienced Lamarckian evolution because phenotypic modifications preceded genotypic modifications, whereas we considered that genes that were highly transcribed in the new niche but were later inactivated obeyed Darwinian rules. We used the total transcript abundances and sequences described for the genes of Mimivirus at the beginning of its laboratory life and after 150 passages in allopatric culture on Acanthamoeba spp. We found a statistically significant positive correlation between the level of gene expression at the beginning of the culture and gene inactivation during the 150 passages. In particular, the mean transcript abundance at baseline was significantly lower for inactivated genes than for unchanged genes (165 ± 589 vs. 470 ± 1,625; p < 1e-3), and the mean transcript levels during the replication cycle of Mimivirus M1 were up to 8.5-fold lower for inactivated genes than for unchanged genes. In addition, proteins tended to be less frequently identified from purified virions in their early life in allopatric laboratory culture if they were encoded by variable genes than if they were encoded by conserved genes (9 vs. 15%; p = 0.062). Finally, Lamarckian evolution represented the evolutionary process encountered by 63% of the inactivated genes. Such observations may be explained by the lower level of DNA repair of useless genes.

Keywords: Darwinian evolution; Lamarckian evolution; Mimivirus; allopatry; gene expression profile; genome reduction; transcription profile.

Figure 1

A schematic diagram of the major steps and causes and effects in Darwinian and Lamarckian evolution. In Darwinian evolution (left), genotypic change precedes phenotypic change, whereas these changes occur in the opposite order in Lamarckian evolution (right).

Figure 2

A schematic diagram of the collection, isolation, and experiments conducted for Mimivirus and Mamavirus.

Figure 3

A schematic diagram of the evolution of the gene content of Mimivirus during allopatric laboratory culture on amoebae. The diagram shows the transcript abundance for Mimivirus M1 genes and the proportions of inactivated genes after 150 passages.

Figure 4

The distribution of transcript abundance for Mimivirus M1 genes according to the number of differences between the nucleotide sequences of the Mimivirus M4 and M1 genes. A difference corresponds to the presence of different nucleotides at the same position within a pairwise alignment provided by BLAST for the nucleotide sequences of corresponding genes of Mimivirus M1 and Mimivirus M4.

Figure 5

The distribution of transcript abundance in Mimivirus M1 for different groups/subgroups of genes defined based on their variability and evolution during 150 passages in allopatric laboratory culture on amoebae. The horizontal bars indicate the mean values for each group/subgroup.

Figure 6

The ratio of the mean transcript abundance in Mimivirus M1 between unchanged and inactivated genes during allopatric laboratory culture on amoebae.

Figure 7

The distribution of unchanged, variable, and inactivated genes after 150 passages in allopatric laboratory culture on amoebae per each 10 centiles of transcript abundance, calculated for all Mimivirus M1 genes.

Figure A1

The distribution of transcript abundance of Mimivirus M1 genes for unchanged, variable, and inactivated genes after 150 passages in allopatric laboratory culture on amoebae.

Figure A2

The distribution along the Mimivirus M1 genome of the transcript abundance of Mimivirus M1 genes and the nucleotide variability for the same genes in Mimivirus M1 and M4. For both parameters, the mean values for a sliding window of 10 genes and a step of 1 gene are represented. The variability was defined as the number of variable positions within genes. The yellow boxes toward the tips of the genome indicate large deletions encountered by the genome of Mimivirus during allopatric laboratory culture on amoebae, as previously reported (Boyer et al., 2011).