On 2013 Nov 09, Claudiu Bandea commented:

What is a virus?

With 1 µm in length and 0.5 µm in diameter, and a genome coding for more than 2500 putative proteins, the intriguing parasites isolated in Acanthamoeba cultures by Philippe et al. (1) dwarf numerous cellular microorganisms, including many eukaryotic microbes. To confirm microscopic observations that these parasitic organisms, labeled Pandoraviruses, are indeed viruses, Philippe et al., used negative defining criteria based on absence of components for three “basic cellular functions”: (i) production of adenosine 5’-triphosphate, (ii) binary fission, and (iii) translational machinery.

However, many cellular microorganisms lack the components for production of adenosine 5’-triphosphate (2, 3), and some, such as yeast (4), produce multiple internal spores by de novo assembly of cellular membranes, rather than by binary fission. Moreover, some cellular microorganisms (2) don’t encode a full set of translational components, and many viruses produce translational components (e. g. tRNAs, amino acid-tRNA ligases, eIF4E translation initiation factor). Therefore, the negative criteria used by Philippe et al. for defining viruses, which were also emphasized in the accompanying article (5) and in ‘About the Cover’ (Science, 19 July 2013), do not differentiate between viruses and cellular microorganisms.

Are Pandoraviruses viruses? Addressing this question might require a fundamental re-evaluation of the conventional view about the nature of viruses (6-9), not only in light of the vast amounts of data and knowledge about their composition, life cycle and evolution, but also in context of the expanding data and knowledge about the diversity of cellular microorganisms (2,3). One of the fundamental features that differentiate viruses from parasitic or symbiotic cellular organisms is that, during their intracellular development, viruses have their genome and other specific components more or less ‘free’ or dispersed within the host cell, whereas intracellular bacterial, archaeal and eukaryotic microorganisms maintain a cellular membrane and cellular organization throughout their life cycle.

This view on the fundamental nature of viruses is consistent with a radical evolutionary model proposing that viral lineages originated from parasitic cellular species that started their intracellular development by fusing with their host cell (6, 8). By discarding their cellular membrane within their particular environment, the host cell, these novel parasites increased their access to host’s resources, including the translation machinery. Nevertheless, after synthesizing their specific molecules and replicating their genome using the resources found in their intracellular environment, the parasites produced spore-like transmissible forms, which started a new life cycle by fusing with other host cells.

Although the life cycle of many extant viruses, including Poxviruses and Mimivirus, fully support the fusion model on the origin of viral lineages (8), Pandoraviruses represent overwhelming evidence. There is also strong evidence, including the absence of ribosomes, that some previously isolated parasitic microorganisms, such as KC5/2 (10) and KLaHel endocytobionts (11), are complex viral organisms. However, as previously discussed (8), there are many other complex parasitic species that are genuine viral organisms although they still produce ribosomes or ribosomal remnants.

The absence of a cellular membrane within the host cell has presented the viral lineages with unique evolutionary opportunities, not readily available for their relatives that maintained a cellular membrane during their intracellular development. However, similar to all intracellular parasitic or symbiotic cellular species, which have been evolving towards a smaller genome (2, 3), the viral lineages have diversified by reductive evolution into a myriad of viruses with smaller genome and diverse life cycles (6, 8). One of the most remarkable implications of the fusion model is that numerous cellular species have evolved into viral lineages throughout the history of life and that this process is still active.

This radical evolutionary theory on the nature and origin of viral lineages also addresses one of the most persisting and intriguing issue in biology, an issue that has puzzled scientists and philosophers for more than a century: are viruses alive? If viral lineages originated from cellular microorganisms as proposed in the fusion model, then, there are few remaining arguments against their living status and their rightful place on the Tree of Life (8).

References

(1) Philippe N. et al., Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281, (2013). Philippe N, 2013

(2) Keeling PJ, Corradi N. Shrink it or lose it: balancing loss of function with shrinking genomes in the microsporidia. Virulence 2, 67, (2011). Keeling PJ, 2011

(3) McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nature reviews. Microbiology 10, 13, (2011). McCutcheon JP, 2011

(4) Neiman AM. Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189, 737, (2011). Neiman AM, 2011

(5) Pennisi E. Microbiology. Ever-bigger viruses shake tree of life. Science 341, 226, (2013). Pennisi E, 2013

(6) Bandea CI. A new theory on the origin and the nature of viruses. Journal of Theoretical Biology 105, 591, (1983). Bândea CI, 1983

(7) Claverie JM. Viruses take center stage in cellular evolution. Genome Biol. 7, 110, (2006). Claverie JM, 2006

(8) Bandea CI. The origin and evolution of viruses as molecular organisms. Nature Precedings: http://precedings.nature.com/documents/3886/version/1; (2009).

(9) Forterre P. Giant viruses: conflicts in revisiting the virus concept. Intervirology 53, 362, (2010). Forterre P, 2010

(10) Hoffmann R, Michel R, Müller KD, Schmid EN. Archaea-like endocytobiotic organisms isolated from Acanthamoeba sp. (Gr II). Endocytobiosis & Cell Res.12, 185, (1998). http://zs.thulb.uni-jena.de/servlets/MCRFileNodeServlet/jportal_derivate_00100794/ECR_12_1997_185-188_Hoffmann.pdf

(11) Scheid P, Zoller L, Pressmar S, Richard G, Michel R. An extraordinary endocytobiont in Acanthamoeba sp. isolated from a patient with keratitis. Parasitol. Res.102, 945, (2008). Scheid P, 2008

On 2013 Nov 09, Claudiu Bandea commented:

What is a virus?

With 1 µm in length and 0.5 µm in diameter, and a genome coding for more than 2500 putative proteins, the intriguing parasites isolated in Acanthamoeba cultures by Philippe et al. (1) dwarf numerous cellular microorganisms, including many eukaryotic microbes. To confirm microscopic observations that these parasitic organisms, labeled Pandoraviruses, are indeed viruses, Philippe et al., used negative defining criteria based on absence of components for three “basic cellular functions”: (i) production of adenosine 5’-triphosphate, (ii) binary fission, and (iii) translational machinery.

However, many cellular microorganisms lack the components for production of adenosine 5’-triphosphate (2, 3), and some, such as yeast (4), produce multiple internal spores by de novo assembly of cellular membranes, rather than by binary fission. Moreover, some cellular microorganisms (2) don’t encode a full set of translational components, and many viruses produce translational components (e. g. tRNAs, amino acid-tRNA ligases, eIF4E translation initiation factor). Therefore, the negative criteria used by Philippe et al. for defining viruses, which were also emphasized in the accompanying article (5) and in ‘About the Cover’ (Science, 19 July 2013), do not differentiate between viruses and cellular microorganisms.

Are Pandoraviruses viruses? Addressing this question might require a fundamental re-evaluation of the conventional view about the nature of viruses (6-9), not only in light of the vast amounts of data and knowledge about their composition, life cycle and evolution, but also in context of the expanding data and knowledge about the diversity of cellular microorganisms (2,3). One of the fundamental features that differentiate viruses from parasitic or symbiotic cellular organisms is that, during their intracellular development, viruses have their genome and other specific components more or less ‘free’ or dispersed within the host cell, whereas intracellular bacterial, archaeal and eukaryotic microorganisms maintain a cellular membrane and cellular organization throughout their life cycle.

This view on the fundamental nature of viruses is consistent with a radical evolutionary model proposing that viral lineages originated from parasitic cellular species that started their intracellular development by fusing with their host cell (6, 8). By discarding their cellular membrane within their particular environment, the host cell, these novel parasites increased their access to host’s resources, including the translation machinery. Nevertheless, after synthesizing their specific molecules and replicating their genome using the resources found in their intracellular environment, the parasites produced spore-like transmissible forms, which started a new life cycle by fusing with other host cells.

Although the life cycle of many extant viruses, including Poxviruses and Mimivirus, fully support the fusion model on the origin of viral lineages (8), Pandoraviruses represent overwhelming evidence. There is also strong evidence, including the absence of ribosomes, that some previously isolated parasitic microorganisms, such as KC5/2 (10) and KLaHel endocytobionts (11), are complex viral organisms. However, as previously discussed (8), there are many other complex parasitic species that are genuine viral organisms although they still produce ribosomes or ribosomal remnants.

The absence of a cellular membrane within the host cell has presented the viral lineages with unique evolutionary opportunities, not readily available for their relatives that maintained a cellular membrane during their intracellular development. However, similar to all intracellular parasitic or symbiotic cellular species, which have been evolving towards a smaller genome (2, 3), the viral lineages have diversified by reductive evolution into a myriad of viruses with smaller genome and diverse life cycles (6, 8). One of the most remarkable implications of the fusion model is that numerous cellular species have evolved into viral lineages throughout the history of life and that this process is still active.

This radical evolutionary theory on the nature and origin of viral lineages also addresses one of the most persisting and intriguing issue in biology, an issue that has puzzled scientists and philosophers for more than a century: are viruses alive? If viral lineages originated from cellular microorganisms as proposed in the fusion model, then, there are few remaining arguments against their living status and their rightful place on the Tree of Life (8).

References

(1) Philippe N. et al., Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341, 281, (2013). Philippe N, 2013

(2) Keeling PJ, Corradi N. Shrink it or lose it: balancing loss of function with shrinking genomes in the microsporidia. Virulence 2, 67, (2011). Keeling PJ, 2011

(3) McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nature reviews. Microbiology 10, 13, (2011). McCutcheon JP, 2011

(4) Neiman AM. Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189, 737, (2011). Neiman AM, 2011

(5) Pennisi E. Microbiology. Ever-bigger viruses shake tree of life. Science 341, 226, (2013). Pennisi E, 2013

(6) Bandea CI. A new theory on the origin and the nature of viruses. Journal of Theoretical Biology 105, 591, (1983). Bândea CI, 1983

(7) Claverie JM. Viruses take center stage in cellular evolution. Genome Biol. 7, 110, (2006). Claverie JM, 2006

(8) Bandea CI. The origin and evolution of viruses as molecular organisms. Nature Precedings: http://precedings.nature.com/documents/3886/version/1; (2009).

(9) Forterre P. Giant viruses: conflicts in revisiting the virus concept. Intervirology 53, 362, (2010). Forterre P, 2010

(10) Hoffmann R, Michel R, Müller KD, Schmid EN. Archaea-like endocytobiotic organisms isolated from Acanthamoeba sp. (Gr II). Endocytobiosis & Cell Res.12, 185, (1998). http://zs.thulb.uni-jena.de/servlets/MCRFileNodeServlet/jportal_derivate_00100794/ECR_12_1997_185-188_Hoffmann.pdf

(11) Scheid P, Zoller L, Pressmar S, Richard G, Michel R. An extraordinary endocytobiont in Acanthamoeba sp. isolated from a patient with keratitis. Parasitol. Res.102, 945, (2008). Scheid P, 2008