A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells

Erdmann, Susanne; Tschitschko, Bernhard; Zhong, Ling; Raftery, Mark J.; Cavicchioli, Ricardo

doi:10.1038/s41564-017-0009-2

Cited by 116 publications

(170 citation statements)

References 63 publications

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“…The non‐lytic pleomorphic virus life cycle starts with fusion between the viral and host membranes and they exit the host cell most probably by budding, preserving the host membrane integrity (Svirskaite et al ., ; El Omari et al ., ). Their simplistic mechanism of nucleic acid transmission resembles the function of the recently described ‘infectious’ plasmid membrane vesicles isolated from Antarctic species of haloarchaea (Erdmann et al ., ), supporting the tight evolutionary relationships between viruses and non‐viral mobile genetic elements (Iranzo et al ., ). Pleolipoviruses share a conserved core of four to five genes, mainly encoding major structural proteins of which one is the spike protein responsible for host attachment and membrane fusion (Pietilä et al ., ; Sencilo et al ., ; El Omari et al ., ).…”

Section: Introductionmentioning

confidence: 62%

Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species

Mizuno

Prajapati

Lucas-Staat

et al. 2019

Environmental Microbiology

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Summary The diversity of archaeal viruses is severely undersampled compared with that of viruses infecting bacteria and eukaryotes, limiting our understanding on their evolution and environmental impacts. Here, we describe the isolation and characterization of four new viruses infecting halophilic archaea from the saline Lake Retba, located close to Dakar on the coast of Senegal. Three of the viruses, HRPV10, HRPV11 and HRPV12, have enveloped pleomorphic virions and should belong to the family Pleolipoviridae, whereas the forth virus, HFTV1, has an icosahedral capsid and a long non‐contractile tail, typical of bacterial and archaeal members of the order Caudovirales. Comparative genomic and phylogenomic analyses place HRPV10, HRPV11 and HRPV12 into the genus Betapleolipovirus, whereas HFTV1 appears to be most closely related to the unclassified Halorubrum virus HRTV‐4. Differently from HRTV‐4, HFTV1 encodes host‐derived minichromosome maintenance helicase and PCNA homologues, which are likely to orchestrate its genome replication. HFTV1, the first archaeal virus isolated on a Haloferax strain, could also infect Halorubrum sp., albeit with an eightfold lower efficiency, whereas pleolipoviruses nearly exclusively infected autochthonous Halorubrum strains. Mapping of the metagenomic sequences from this environment to the genomes of isolated haloarchaeal viruses showed that these known viruses are underrepresented in the available viromes.

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Section: Introductionmentioning

confidence: 62%

Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species

Mizuno

Prajapati

Lucas-Staat

et al. 2019

Environmental Microbiology

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Section: Discussionmentioning

confidence: 97%

“…The genetic organization of pT26‐2 is reminiscent of that of the infectious plasmid pR1SE recently isolated from vesicles of the halophilic archaeon Halorubrum lacusprofundi R1SE, albeit without any direct sequence conservation (Erdmann et al ., ). It was experimentally shown that pR1SE can promote its own transfer between cells via extracellular vesicles which contain multiple transmembrane proteins encoded by the plasmid itself (Erdmann et al ., ). Other plasmids in Thermococcales species, such as the pTN3, have been shown to use membrane vesicles to transfer horizontally (Gaudin et al ., ), and two species containing integrated plasmids of the pT26‐2 family, Thermococcus gammatolerans and Pyrococcus horikoshii , were shown to produce membrane vesicles containing cellular DNA (Soler et al ., ).…”

Section: Discussionmentioning

confidence: 97%

The global distribution and evolutionary history of the pT26‐2 archaeal plasmid family

Badel

Erauso

Gomez

et al. 2019

Environmental Microbiology

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Summary Although plasmids play an important role in biological evolution, the number of plasmid families well‐characterized in terms of geographical distribution and evolution remains limited, especially in archaea. Here, we describe the first systematic study of an archaeal plasmid family, the pT26‐2 plasmid family. The in‐depth analysis of the distribution, biogeography and host–plasmid co‐evolution patterns of 26 integrated and 3 extrachromosomal plasmids of this plasmid family shows that they are widespread in Thermococcales and Methanococcales isolated from around the globe but are restricted to these two orders. All members of the family share seven core genes but employ different integration and replication strategies. Phylogenetic analysis of the core genes and CRISPR spacer distribution suggests that plasmids of the pT26‐2 family evolved with their hosts independently in Thermococcales and Methanococcales, despite these hosts exhibiting similar geographic distribution. Remarkably, core genes are conserved even in integrated plasmids that have lost replication genes and/or replication origins suggesting that they may be beneficial for their hosts. We hypothesize that the core proteins encode for a novel type of DNA/protein transfer mechanism, explaining the widespread oceanic distribution of the pT26‐2 plasmid family.

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“…Cytoskeletal proteins often have multiple functions, and are adapted for use in various biological contexts. A recent study analysing the composition of membrane vesicles (MVs) of a haloarchaeal species, Halorubrum lacusprofundi, revealed the presence of a CetZ1 homolog in MVs and specialised plasmid-containing membrane vesicles (PVs) [47]. This protein was significantly more enriched in purified vesicles when compared with membrane fractions prepared from the host, suggesting that it might play a role in membrane vesicle formation or structure [47].…”

Section: Expression Of a Cetz1mentioning

confidence: 99%

Archaeal cell biology: diverse functions of tubulin-like cytoskeletal proteins at the cell envelope

Liao

Ithurbide

Silva

et al. 2018

Emerging Topics in Life Sciences

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The tubulin superfamily of cytoskeletal proteins is widespread in all three domains of life — Archaea, Bacteria and Eukarya. Tubulins build the microtubules of the eukaryotic cytoskeleton, whereas members of the homologous FtsZ family construct the division ring in prokaryotes and some eukaryotic organelles. Their functions are relatively poorly understood in archaea, yet these microbes contain a remarkable diversity of tubulin superfamily proteins, including FtsZ for division, a newly described major family called CetZ that is involved in archaeal cell shape control, and several other divergent families of unclear function that are implicated in a variety of cell envelope-remodelling contexts. Archaeal model organisms, particularly halophilic archaea such as Haloferax volcanii, have sufficiently developed genetic tools and we show why their large, flattened cells that are capable of controlled differentiation are also well suited to cell biological investigations by live-cell high-resolution light and electron microscopy. As most archaea only have a glycoprotein lattice S-layer, rather than a peptidoglycan cell wall like bacteria, the activity of the tubulin-like cytoskeletal proteins at the cell envelope is expected to vary significantly, and may involve direct membrane remodelling or directed synthesis or insertion of the S-layer protein subunits. Further studies of archaeal cell biology will provide fresh insight into the evolution of cells and the principles in common to their fundamental activities across the full spectrum of cellular life.

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A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells

Cited by 116 publications

References 63 publications

Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species

Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species

The global distribution and evolutionary history of the pT26‐2 archaeal plasmid family

Archaeal cell biology: diverse functions of tubulin-like cytoskeletal proteins at the cell envelope

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