Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment

Ogata, Hiroyuki; Ray, Jessica L.; Toyoda, Kensuke; Sandaa, Ruth Anne; Nagasaki, Keisuke; Bratbak, Gunnar; Claverie, Jean‐Michel

doi:10.1038/ismej.2010.210

Cited by 73 publications

(102 citation statements)

References 59 publications

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“…Megavirus exhibits orthologs to all these previously identified genes, including a specific type of mismatch repair enzyme MutS (mg543) common to large DNA viruses and specifically abundant in the marine environment (26). In addition, Megavirus exhibits a DNA photolyase (mg779), an enzyme using the energy of light to repair thymidine dimers.…”

Section: Resultsmentioning

confidence: 99%

Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae

Arslan

Legendre

Seltzer

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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312

334

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Mimivirus, a DNA virus infecting acanthamoeba, was for a long time the largest known virus both in terms of particle size and gene content. Its genome encodes 979 proteins, including the first four aminoacyl tRNA synthetases (ArgRS, CysRS, MetRS, and TyrRS) ever found outside of cellular organisms. The discovery that Mimivirus encoded trademark cellular functions prompted a wealth of theoretical studies revisiting the concept of virus and associated large DNA viruses with the emergence of early eukaryotes. However, the evolutionary significance of these unique features remained impossible to assess in absence of a Mimivirus relative exhibiting a suitable evolutionary divergence. Here, we present Megavirus chilensis, a giant virus isolated off the coast of Chile, but capable of replicating in fresh water acanthamoeba. Its 1,259,197-bp genome is the largest viral genome fully sequenced so far. It encodes 1,120 putative proteins, of which 258 (23%) have no Mimivirus homologs. The 594 Megavirus/Mimivirus orthologs share an average of 50% of identical residues. Despite this divergence, Megavirus retained all of the genomic features characteristic of Mimivirus, including its cellular-like genes. Moreover, Megavirus exhibits three additional aminoacyl-tRNA synthetase genes (IleRS, TrpRS, and AsnRS) adding strong support to the previous suggestion that the Mimivirus/Megavirus lineage evolved from an ancestral cellular genome by reductive evolution. The main differences in gene content between Mimivirus and Megavirus genomes are due to (i) lineages specific gains or losses of genes, (ii) lineage specific gene family expansion or deletion, and (iii) the insertion/migration of mobile elements (intron, intein).Mimiviridae | DNA virus phylogeny | girus | viral translation | tree of life

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Section: Resultsmentioning

confidence: 99%

Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae

Arslan

Legendre

Seltzer

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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312

334

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“…exoDNase (PgV94, with a homolog in CroV), and a mismatch repair enzyme (PgV283) of a type (MutS8) uniquely found in OLPV1 and -2, Phaeocystis pouchetii virus, and Pyramimonas orientalis virus (22). The PgV genome is also rich in putative ribonucleases such as a bacterial ribonuclease HII-like (PgV121, with homologs in CroV and EhV), a RNase T-like (PgV123, with homologs found in many viruses and phage but very divergent in Megavirus and Mimivirus), and a PIN-domain containing RNase H (PgV303, with homologs in CroV and phages).…”

Section: Resultsmentioning

confidence: 99%

Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes

Santini

Jeudy

Bartoli

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Large dsDNA viruses are involved in the population control of many globally distributed species of eukaryotic phytoplankton and have a prominent role in bloom termination. The genus Phaeocystis ( Haptophyta , Prymnesiophyceae ) includes several high-biomass-forming phytoplankton species, such as Phaeocystis globosa , the blooms of which occur mostly in the coastal zone of the North Atlantic and the North Sea. Here, we report the 459,984-bp-long genome sequence of P. globosa virus strain PgV-16T, encoding 434 proteins and eight tRNAs and, thus, the largest fully sequenced genome to date among viruses infecting algae. Surprisingly, PgV-16T exhibits no phylogenetic affinity with other viruses infecting microalgae (e.g., phycodnaviruses), including those infecting Emiliania huxleyi , another ubiquitous bloom-forming haptophyte. Rather, PgV-16T belongs to an emerging clade (the Megaviridae) clustering the viruses endowed with the largest known genomes, including Megavirus, Mimivirus (both infecting acanthamoeba), and a virus infecting the marine microflagellate grazer Cafeteria roenbergensis . Seventy-five percent of the best matches of PgV-16T–predicted proteins correspond to two viruses [Organic Lake phycodnavirus (OLPV)1 and OLPV2] from a hypersaline lake in Antarctica (Organic Lake), the hosts of which are unknown. As for OLPVs and other Megaviridae, the PgV-16T sequence data revealed the presence of a virophage-like genome. However, no virophage particle was detected in infected P. globosa cultures. The presence of many genes found only in Megaviridae in its genome and the presence of an associated virophage strongly suggest that PgV-16T shares a common ancestry with the largest known dsDNA viruses, the host range of which already encompasses the earliest diverging branches of domain Eukarya.

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“…The first involved a C-terminal fusion to a GIY-YIG homing endonuclease domain (VI; Abdelnoor et al, 2006), and the second involved the inclusion of hydrophobic stretches within the region linking essential DNA binding (I) and ATPase (V) domains. These and other sequence features distinguish the plant protein from any other MutS homolog yet identified (Ogata et al, 2011) and presumably confer unique functional properties.…”

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confidence: 99%

The Chloroplast Triggers Developmental Reprogramming When MUTS HOMOLOG1 Is Suppressed in Plants

Santamaria

Virdi

et al. 2012

Plant Physiology

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Multicellular eukaryotes demonstrate nongenetic, heritable phenotypic versatility in their adaptation to environmental changes. This inclusive inheritance is composed of interacting epigenetic, maternal, and environmental factors. Yet-unidentified maternal effects can have a pronounced influence on plant phenotypic adaptation to changing environmental conditions. To explore the control of phenotypy in higher plants, we examined the effect of a single plant nuclear gene on the expression and transmission of phenotypic variability in Arabidopsis (Arabidopsis thaliana). MutS HOMOLOG1 (MSH1) is a plant-specific nuclear gene product that functions in both mitochondria and plastids to maintain genome stability. RNA interference suppression of the gene elicits strikingly similar programmed changes in plant growth pattern in six different plant species, changes subsequently heritable independent of the RNA interference transgene. The altered phenotypes reflect multiple pathways that are known to participate in adaptation, including altered phytohormone effects for dwarfed growth and reduced internode elongation, enhanced branching, reduced stomatal density, altered leaf morphology, delayed flowering, and extended juvenility, with conversion to perennial growth pattern in short days. Some of these effects are partially reversed with the application of gibberellic acid. Genetic hemicomplementation experiments show that this phenotypic plasticity derives from changes in chloroplast state. Our results suggest that suppression of MSH1, which occurs under several forms of abiotic stress, triggers a plastidial response process that involves nongenetic inheritance.

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Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment

Cited by 73 publications

References 59 publications

Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae

Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae

Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes

The Chloroplast Triggers Developmental Reprogramming When MUTS HOMOLOG1 Is Suppressed in Plants

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