Evolution of Genomic Base Composition: From Single Cell Microbes to Multicellular Animals

Bohlin, Jon; Pettersson, John H.‐O.

doi:10.1016/j.csbj.2019.03.001

Cited by 29 publications

(38 citation statements)

References 125 publications

(222 reference statements)

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“…The accumulation of LCRs is likely to reflect weak selection in small populations in the course of reductive evolution (22,23). A similar phenomenon is observed in many parasitic bacteria with small, degraded genomes (24). The LCRs in virion proteins could substantially contribute to antigenic variation (25).…”

Section: Resultssupporting

confidence: 66%

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

Subramaniam

Behringer

Yutin

et al. 2020

mBio

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Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbean spiny lobster (Panulirus argus) from the Caribbean Sea. Recently, related viruses, Dikerogammarus haemobaphes virus 1 (DhV1) and Carcinus maenas virus 1 (CmV1), have been detected in the demon shrimp (Dikerogammarus haemobaphes) and the European shore crab (Carcinus maenas), respectively, from sites in the United Kingdom. The virion morphology of these crustacean viruses is similar to that of iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNA viruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleus rather than in the cytoplasm. To date, these crustacean viruses have remained unclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, we sequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genome analysis shows that these crustacean virus genomes encode the 10 hallmark proteins previously described for the NCLDVs of eukaryotes, strongly suggesting that they are members of this group. With a size range of 70 to 74 kb, these are the smallest NCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences, and the accumulation of low-complexity sequences reflect the extreme degradation of the genomes of these “minimal” NCLDVs rather than any direct relationship with the NCLDV ancestor. Phylogenomic analysis supports the classification of these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pitho-irido-Marseille branch of the NCLDVs. IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansion of the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) of eukaryotes, which include giant viruses of protists and important pathogens of vertebrates, such as poxviruses. However, the characterization of viruses from nonmodel hosts still lags behind. We sequenced the complete genomes of three viruses infecting crustaceans, the Caribbean spiny lobster, demon shrimp, and European shore crab. These viruses have the smallest genomes among the known NCLDVs, with losses of many core genes, some of which are shared with iridoviruses. The deterioration of the transcription apparatus is compatible with microscopic and ultrastructural observations indicating that these viruses replicate in the nucleus of infected cells rather than in the cytoplasm. Phylogenomic analysis indicates that these viruses are sufficiently distinct from all other NCLDVs to justify the creation of a separate family, for which we propose the name “Mininucleoviridae” (i.e., small viruses reproducing in the cell nucleus).

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Section: Resultssupporting

confidence: 66%

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

Subramaniam

Behringer

Yutin

et al. 2020

mBio

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“…between k-mers within a given organism, or across species have not yet received convincing biological explanations 32,33 . This suggests that profound and unexpected biological insights may one day come out from the analysis of k-mer frequencies, and in particular from their most improbable fluctuations.…”

Section: Discussionmentioning

confidence: 99%

A Puzzling Anomaly in the 4-Mer Composition of the Giant Pandoravirus Genomes Reveals a Stringent New Evolutionary Selection Process

Poirot

Jeudy

Abergel

et al. 2019

J Virol

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Pandoraviridae is a rapidly growing family of giant viruses, all of which have been isolated using laboratory strains of Acanthamoeba. The genomes of 10 distinct strains have been fully characterized, reaching up to 2.5 Mb in size. These double-stranded DNA genomes encode the largest of all known viral proteomes and are propagated in oblate virions that are among the largest ever described (1.2 μm long and 0.5 μm wide). The evolutionary origin of these atypical viruses is the object of numerous speculations. Applying the chaos game representation to the pandoravirus genome sequences, we discovered that the tetranucleotide (4-mer) “AGCT” is totally absent from the genomes of 2 strains (Pandoravirus dulcis and Pandoravirus quercus) and strongly underrepresented in others. Given the amazingly low probability of such an observation in the corresponding randomized sequences, we investigated its biological significance through a comprehensive study of the 4-mer compositions of all viral genomes. Our results indicate that AGCT was specifically eliminated during the evolution of the Pandoraviridae and that none of the previously proposed host-virus antagonistic relationships could explain this phenomenon. Unlike the three other families of giant viruses (Mimiviridae, Pithoviridae, and Molliviridae) infecting the same Acanthamoeba host, the pandoraviruses exhibit a puzzling genomic anomaly suggesting a highly specific DNA editing in response to a new kind of strong evolutionary pressure. IMPORTANCE Recent years have seen the discovery of several families of giant DNA viruses infecting the ubiquitous amoebozoa of the genus Acanthamoeba. With double-stranded DNA (dsDNA) genomes reaching 2.5 Mb in length packaged in oblate particles the size of a bacterium, the pandoraviruses are currently the most complex and largest viruses known. In addition to their spectacular dimensions, the pandoraviruses encode the largest proportion of proteins without homologs in other organisms, which is thought to result from a de novo gene creation process. While using comparative genomics to investigate the evolutionary forces responsible for the emergence of such an unusual giant virus family, we discovered a unique bias in the tetranucleotide composition of the pandoravirus genomes that can result only from an undescribed evolutionary process not encountered in any other microorganism.

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“…Many bacteria subjected to relaxed selection are often intracellular and, in general, reside or replicate within the infected host cell with a limited chance of recombining or exchanging DNA with other bacteria [ 30 , 31 , 32 ]. Moreover, GC to AT mutations have been shown to occur approximately twice as often as AT to GC mutations and seem to be more readily fixed within the genome [ 33 , 34 ].…”

Section: Discussionmentioning

confidence: 99%

Differences in Blood-Derived Francisella tularensis Type B Strains from Clinical Cases of Tularemia

et al. 2020

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Francisella tularensis can cause the zoonotic disease tularemia and is partitioned into subspecies due to differences in chromosomal organization and virulence. The subspecies holarctica (type B) is generally considered more clonal than the other subpopulations with moderate virulence compared to the hypervirulent A.I clade. We performed whole genome sequencing (WGS) on six type B strains isolated from the blood of patients with tularemia within a one-year period from the same United States region, to better understand the associated pathogenicity. The WGS data were compared to the prototype strain for this subspecies, specifically FSC200, which was isolated from a patient with tularemia in Europe. These findings revealed 520–528 single nucleotide polymorphisms (SNPs) between the six United States type B strains compared to FSC200, with slightly higher A+T content in the latter strain. In contrast, comparisons between the six type B isolates showed that five of the six type B isolates had only 4–22 SNPs, while one of the strains had 47–53 SNPs. Analysis of SNPs in the core genome for the six United States type B isolates and the FSC200 strain gave similar results, suggesting that some of these mutations may have been nonsynonymous, resulting in altered protein function and pathogenicity.

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Evolution of Genomic Base Composition: From Single Cell Microbes to Multicellular Animals

Cited by 29 publications

References 125 publications

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

A Puzzling Anomaly in the 4-Mer Composition of the Giant Pandoravirus Genomes Reveals a Stringent New Evolutionary Selection Process

Differences in Blood-Derived Francisella tularensis Type B Strains from Clinical Cases of Tularemia

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