On 2024-01-03 01:25:21, user Claudiu Bandea wrote:
New evidence supports the hypothesis that Borgs are incipient viral lineages <br />
(Claudiu Bandea, Dec 28, 2023)
The discovery of Borgs as giant extrachromosomal elements, presumably inhabiting Methanoperedens archaea, was first published in 2021, in bioRxiv [1]. More than a year later, the study was also published in Nature under a slightly different title and content [2]. The study, which reported the sequencing and analysis of more than a dozen Borg genomes (661,708 to 918,293 kb in length), including four genomes that were fully curated and analyzed, found no evidence of viral characteristics.
On the basis of these results, the authors asserted the following: “We can neither prove that they are archaeal viruses or plasmids or minichromosomes, nor prove that they are not. Although they may ultimately be classified as megaplasmids, they are clearly different from anything that has been previously reported” (all quotes in Italics) [2]. This statement raises a critical question: what kind of evidence would warrant the classification of Borgs as viruses, megaplasmids, or minichromosomes? Surprisingly, the authors did not address this essential issue.
Despite the Borgs’ apparent lack of viral characteristics, in a commentary entitled “Will Borgs Illuminate the Evolutionary Origin of Ancestral Viral Lineages?” [3], I suggested that Borgs are incipient viral lineages and, thus, illuminate one of the biggest mysteries in biology – the origin of viruses.
Remarkably, in a new article published in bioRxiv by the same group [4], we learn that, after all, Borgs do encode numerous putative viral proteins, including several capsid proteins, as well as proteins implicated in the replication, recombination, and spread of Borgs to new host cells. The new study presents additional evidence, including a high ratio between the number of Borgs and their presumed Methanoperedens hosts and a distinct methylation pattern of their genomes, which point to an extracellular stage in the Borgs’ life cycle and to their viral nature.
As I outlined in my previous commentary [3], the rationale for proposing that Borgs might be incipient viral lineages, even in the absence of the conventional physical, biochemical, and biological features historically used to define viruses (see below), was rooted in the Fusion Hypothesis regarding the evolutionary origin of viruses [5-7].
According to this hypothesis, the ancestral or incipient viral lineages originated from ecto- or endo-symbiotic or parasitic cellular lineages that fused with their host cells. By fusing with their host cells and discarding their cellular membrane, these lineages transitioned to new type of biological organization and structure (see below), which gave them full access to the host cell resources, including the host’s ribosomes and other components of the translation machinery. After synthesizing their specific molecules and replicating their genome using the resources found in their special environmental niche (i.e., the host cell), this new type of organisms induced the assembly and morphogenesis of reproductive, transmissible forms, which started a new life cycle by fusing with other host cells.
The absence of a cellular membrane within the host cell presented the incipient viral lineages with unique reductive evolutionary opportunities, not readily available for parasitic or symbiotic cellular lineages, which led to a myriad of new viruses with diverse lifestyles and biochemical composition. As outlined below, the fusion model completely changes the conventional views regarding the nature of viruses, their evolutionary origin, and their role in shaping the evolution of cellular lineages.
The nature of viruses
Ever since viruses were identified more than a century ago as infectious agents that passed through filters thought at that time to retain all microorganisms, they have been conceptually identified with the virus particles, or virions - the transmissible infectious forms in the viral life cycle. Accordingly, viruses have been defined based on the physical, biochemical, and biological properties of these particles, as illustrated in virtually all scientific literature and textbooks to date.
For example, in his seminal book, The Molecular Biology of the Gene, James Watson, who was highly familiar with nucleic acids, as well as with viruses [8], wrote: “All viruses differ fundamentally from cells, which have both DNA and RNA, in that viruses contain only one type of nucleic acid, which may be either DNA or RNA” [9]. A decade later, in A Dictionary of Virology, viruses were defined as “Infectious units consisting of either RNA or DNA enclosed in a protective coat” [10], and in the 1990s, a classic microbiology textbook, Zinsser Microbiology, stated that viruses “consist of a genome, either RNA or DNA, that is surrounded by a protective protein shell” [11].
Surely, the authors of these scientific publications were fully aware that, during the intracellular stage of their life cycle, many viruses, such as the “DNA viruses” and retroviruses, have both type of nuclei acids, DNA as well as RNA, and that many viruses are much more complex than a nucleic acid wrapped in a protein coat. Yet, all these renowned scientists fell victim to the concept of viruses as virus particles and used the physical, biochemical, and biological properties of these particles to define viruses. This is a strong example of the power of concepts in science. A concept that clearly misrepresents the experimental findings and observations can persist for decades, or, as in the case of viruses, for more than a century.
Forty years ago, in 1983, I proposed that, like many parasitic cellular lineages, viruses pass in their life cycle through two phenotypically distinct stages: the extracellular, reproductive forms represented by the virus particles, and the intracellular forms in which the viral molecules and components are “free” or dispersed within their host cell [5].
The viral particles are highly specialized structures that are used by some viruses for their transmission to new host cells. This role of viral particles in the viral life cycle explains their properties, including their apparent inert status and the presence of only one type of nucleic acid - DNA or RNA. Many viruses, however, do not produce viral particles, using instead alternative modes of transmission [12]. This fact alone indicates that identifying viruses with the virus particles misrepresents their nature. Nevertheless, the fundamental biological properties of viruses, whether they do or do not produce virions, are expressed during the intracellular stage of the viral life cycle, when viruses replicate their genome and synthesize their specific molecules, many of which are not components of the viral particles.
To identify viruses phenotypically during the intracellular stage of their life cycle with the integrative sum of all their molecules, and to differentiate them conceptually from the parasitic lineages that maintain a cellular membrane within the host cell, I proposed the concept of molecular structure and labeled viruses as molecular organisms [5, 6].
Although the concepts of molecular organisms and molecular structure (which, by analogy with the host cell’s cytoplasm, can be called viroplasm) are more suggestively envisioned within the framework of the fusion hypothesis, these concepts are also applicable in context of the other hypotheses regarding the origin and evolution of viruses (see below). Significantly, these concepts set the foundation for including other biological entities, such as plasmids, endogenous viruses, and viroids, within the same domain of biological organization - the viral domain.
In a commentary entitled “What makes a virus a virus?” [13], Roland Wolkowicz and Moselio Schaechter wrote that the identity of viruses as historically conceptualized and defined (i.e., as virus particles) is missing “the most fundamental aspect of what makes a virus a virus: it breaks up and loses its bodily integrity, with its progeny becoming reconstituted after replication from newly synthesized parts” and that “We are surprised from our own experience that the world of virology has not fully embraced this outlook” .
After the discovery of giant viruses, Jean-Michel Claverie asked, “What if we have totally missed the true nature of (at least some) viruses?” [14], and in a series of publications Patrick Forterre and his colleagues have discussed extensively the limitations of the concept of viruses as virus particles and suggested alternative ways to define viruses and to identify them during the intracellular stage of their life cycle [15-18].
As I discussed in the original publication [5], referring to the intracellular stage of viruses as an “eclipse phase,” denoting the “disappearance” of viruses, was confusing. Likewise, identifying viruses with their genome, thereby ignoring the other viral molecules and components, misrepresents their nature. An alternative approach was to no longer refer to a virus as an individual biological entity, but as an integrated virus-host cell system (i.e., the infected cell0. Recently, Patrick Forterre labeled this integrated system with the term “virocell” [15, 17, 18].
This approach was sharply criticized by Purificación López-García and David Moreira on both scientific and epistemological grounds [19, 20], and recently the virocell term was redefined by DeLong et al., [21], but Forterre rebutted the criticism [18].
Nevertheless, these highly relevant discussions bring forward the acute problems with the dogma of viruses as virus particles and stress the need for a new scientific and academic perspective on viruses, which can productively integrate the extraordinary amount of knowledge about viruses and their role in shaping the life and evolution of their hosts and of the ecosystem in which their live [15, 22-30].
The scientific limitations and academic confusion associated with the concept of viruses as virus particles in virology and related biomedical fields [31-33] remain to be fully addressed. However, questioning the validity of this dogma, which has guided several generations of researchers to extraordinary discoveries and progress in virology, is challenging.
The origin and evolution of viruses
As it would be expected, in the context of the dogma of viruses as virus particles, the hypotheses regarding their evolutionary origin focused on the virions and their structure: (i) thePre-cellular or Virus-first Theory suggested that viruses originated from precellular, self-replicating nucleic acids, or replicons, encoding for capsid proteins; (ii) the Endogenous or Escape Hypothesis suggested that viruses originated from cellular genomic sequences, or replicons, encoding for capsid proteins; (iii) and the historical Regressive or Reductive Hypothesis proposed a reductive transition of parasitic cellular lineages, such as bacteria, into nucleocapsid-like structures.
Within the concept of viruses as virus particles, the validity of the regressive hypothesis was questionable as Salvador Luria and James Darnell pointed out more than half a century ago: “The strongest argument against the regressive origin of viruses from cellular parasites is the non-cellular organization of viruses. The viral capsids are morphogenetically analogous to cellular organelles made up of protein subunits, such as bacterial flagella, actin filaments, and the like, and not to cellular membranes.” [34].
Indeed, many parasitic and symbiotic bacteria have a fraction of the genomic and proteomic repertoire of some viruses. For example, several endosymbionts, such as Carsonella, Hodgkinia, and Tremblaya, have a genome that is less than 200 kb and encode less than 200 proteins [35]. Yet, no symbiotic or parasitic bacteria with highly reduced genomes and metabolic capability resemble virus particles.
As predicted by the fusion hypothesis, only symbiotic or parasitic lineages that have a genetic and metabolic system compatible with that of their host cells would be able to fuse with them and transition to a viral type of biological organization. Accordingly, only bacterial, archaeal, and eukaryotic lineages, hosted by bacterial, archaeal, and eukaryotic host cells, respectively, could evolve into viral lineages [6, 7, 36].
Interestingly, numerous symbiotic and parasitic lineages that inhabit their kin and have reduced genomes and metabolic capabilities have been recently discovered, including highly diverse groups of DPANN archaea and CPR bacteria [37-42]. Hypothetically, some of these archaeal and bacterial lineages are in the process of transitioning into incipient viral lineages [6, 36], similar to the putative cellular ancestors of Borgs [3]. Nevertheless, one of the major appeals of the fusion hypothesis is that, unlike the other hypotheses, it can be addressed experimentally, as some members of these groups archaea and bacteria could be developed as fusion model organisms.
Surprisingly, though, the strongest evidence for the fusion hypothesis is found among more complex organisms - the eukaryotes. According to the fusion model, the nucleomorphs, some of which have a very small genome (<1 Mb) [43], originated from algal endosymbionts that fused with their host cells. Although, currently conceptualized as organelle-like entities, the nucleomorphs are genuine molecular organisms that have maintained their nucleus.
Even more surprising is the fact that numerous parasitic algal and fungal lineages have a life cycle and biological organization that, as I previously pointed out [6], represent overwhelming evidence for the fusion hypothesis. Indeed, several obligate parasitic species of red algae fuse with their host cells and use the host resources, including, in my assessment, the host ribosomes and other components of the translational machinery, to synthesize their molecules, replicate their genome, and induce the morphogenesis of spore-like progenies [44-50].
I cannot overemphasize the significance of these discoveries which support the fusion hypothesis and should be considered breakthrough discoveries not only in the field of parasitology, but also in evolutionary science, and biology.
Many viruses have been discovered serendipitously, including the recent finding in Chaetognaths, a small phylum of marine invertebrates, of two complex viruses, which have yet to be characterized at the molecular level [51, 52]. As more investigators become familiar with the fusion hypothesis and its predictions, it is likely that new types of viruses, as well as of new cellular lineages that are transitioning into incipient viral lineage, will be discovered.
Although, similar to tens of thousands of symbiotic and parasitic cellular lineages, the viral lineages have evolved towards reduced genomes and proteomes, there is clear evidence of frequent exchanges of genetic material with their hosts and other coinfecting organisms [6, 7, 53]. Considering also their high mutational rates, the deep phylogenetic analysis of viruses is inherently difficult [54-58]. Therefore, trying to establish deep phylogenetic relationships among viruses, reaching the origin and early evolution of life, is likely to be a futile effort.
The origin of incipient viral lineages from symbiotic or parasitic cellular lineages by a fusion mechanism is consistent with the current sequence-based phylogenetic analysis indicating orthologous relationships between the genes of some complex viruses and those of their hosts. The fusion hypothesis is also consistent with the complex biology and the life cycle of many viruses [59-62]. Also, unlike the virus-first, and the escape hypotheses, which dominate the current scientific literature [57, 63-65], the fusion hypothesis is consistent with the reductive evolution of thousands of endosymbiotic/parasitic microorganisms, which prompts the critical question: Why would viruses evolve in the opposite way?
Unlike the other two hypotheses on the evolutionary origin of viral lineages, the fusion hypothesis also unambiguously addresses one of the most intriguing scientific and philosophical questions: Are viruses alive? If the viral lineages originated from cellular microorganisms as proposed in the fusion model, then, there are few remaining arguments, if any, against their living status and their rightful place on the Tree of Life [5-7, 66-68].
Finally, it is relevant to mention that the fusion model on the origin of viral lineages is an integral part of a broader perspective - the fusion/anti-fusion theory - regarding the origin and evolution of pre-cellular and cellular lineages, including the archaeal, bacterial, and eukaryotic cellular domains and some of their defining characteristics [7]. Many aspects of this unifying theory, which addresses the major transitions in the history of life, including its origin, can be found as discrete published ideas and hypotheses [69-74].
Luria’s Credo: There is an intrinsic simplicity of nature and the ultimate contribution of science resides in the discovery of unifying and simplifying generalization, rather than in the description of isolated situation - in the visualization of simple, overall patterns rather than in the analysis of patchworks [75].
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