Extracellular vesicles of Euryarchaeida: precursor to eukaryotic membrane trafficking

Since their discovery, extracellular vesicles (EVs) have changed our view on how organisms interact with their extracellular world. EVs are able to traffic a diverse array of molecules across different species and even domains, facilitating numerous functions. In this study, we investigate EV production in Haloferax volcanii, as representative for Euryarchaeida. We uncover that EVs enclose RNA, with specific transcripts preferentially enriched, including those with regulatory potential, and conclude that EVs can act as an RNA communication system between haloarchaea. We demonstrate the key role of an EV-associated Ras superfamily GTPase for EV formation in H. volcanii that is also present across other diverse evolutionary branches of Archaea. Ras superfamily GTPases are key players in eukaryotic intracellular vesicle formation and trafficking mechanisms that have been crucial for the emergence of Eukaryotes. Therefore, we propose that archaeal EV formation could reveal insights into the origin of the compartmentalized eukaryotic cell.

[1]  I. Duggin,et al.  Diversity and Potential Multifunctionality of Archaeal CetZ Tubulin-like Cytoskeletal Proteins , 2023, Biomolecules.

[2]  S. Biller,et al.  Characterization of membrane vesicles in Alteromonas macleodii indicates potential roles in their copiotrophic lifestyle , 2022, bioRxiv.

[3]  U. Gophna,et al.  Isolation of a virus causing a chronic infection in the archaeal model organism Haloferax volcanii reveals antiviral activities of a provirus , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[4]  A. Brazma,et al.  The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences , 2021, Nucleic Acids Res..

[5]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation , 2021, Nucleic Acids Res..

[6]  H. Drost,et al.  Sensitive protein alignments at tree-of-life scale using DIAMOND , 2021, Nature Methods.

[7]  P. Forterre,et al.  Archaeal extracellular vesicles are produced in an ESCRT-dependent manner and promote gene transfer and nutrient cycling in extreme environments , 2021, The ISME Journal.

[8]  Sen-Lin Tang,et al.  The Novel Halovirus Hardycor1, and the Presence of Active (Induced) Proviruses in Four Haloarchaea , 2021, Genes.

[9]  Silvio C. E. Tosatto,et al.  The InterPro protein families and domains database: 20 years on , 2020, Nucleic Acids Res..

[10]  S. Chisholm,et al.  Prochlorococcus extracellular vesicles: molecular composition and adsorption to diverse microbes , 2020, bioRxiv.

[11]  S. Martins,et al.  Extracellular Vesicles in Viral Infections: Two Sides of the Same Coin? , 2020, Frontiers in Cellular and Infection Microbiology.

[12]  Vincent J. Denef,et al.  A genomic catalog of Earth’s microbiomes , 2020, Nature Biotechnology.

[13]  E. Ruby,et al.  The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses , 2020, PLoS biology.

[14]  L. Laurent,et al.  RNA delivery by extracellular vesicles in mammalian cells and its applications , 2020, Nature Reviews Molecular Cell Biology.

[15]  P. Forterre,et al.  Vesiduction: the fourth way of HGT. , 2020, Environmental microbiology.

[16]  Donovan H. Parks,et al.  A complete domain-to-species taxonomy for Bacteria and Archaea , 2020, Nature Biotechnology.

[17]  T. Allers,et al.  Haloferax volcanii for biotechnology applications: challenges, current state and perspectives , 2019, Applied Microbiology and Biotechnology.

[18]  A. Marchfelder,et al.  Whole‐genome comparison between the type strain of Halobacterium salinarum (DSM 3754T) and the laboratory strains R1 and NRC‐1 , 2019, MicrobiologyOpen.

[19]  F. Pfeiffer,et al.  Bioinformatic and genetic characterization of three genes localized adjacent to the major replication origin of Haloferax volcanii. , 2019, FEMS microbiology letters.

[20]  Konrad U. Förstner,et al.  Characterization of the transcriptome of Haloferax volcanii, grown under four different conditions, with mixed RNA-Seq , 2019, PloS one.

[21]  S. Albers,et al.  Cyclic nucleotides in archaea: Cyclic di‐AMP in the archaeon Haloferax volcanii and its putative role , 2019, MicrobiologyOpen.

[22]  H. Wienk,et al.  New Insights Into the Polar Lipid Composition of Extremely Halo(alkali)philic Euryarchaea From Hypersaline Lakes , 2019, Front. Microbiol..

[23]  A. Tonevitsky,et al.  Transcriptome of Extracellular Vesicles: State-of-the-Art , 2019, Front. Immunol..

[24]  A. Spang,et al.  Genomic diversity, lifestyles and evolutionary origins of DPANN archaea , 2019, FEMS microbiology letters.

[25]  P. Forterre,et al.  Extracellular membrane vesicles in the three domains of life and beyond , 2018, FEMS microbiology reviews.

[26]  A. Phillippy,et al.  High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries , 2018, Nature Communications.

[27]  V. Orphan,et al.  Metabolic marker gene mining provides insight in global mcrA diversity and, coupled with targeted genome reconstruction, sheds further light on metabolic potential of the Methanomassiliicoccales , 2018, PeerJ.

[28]  A. Vardi,et al.  Extracellular vesicles - new players in cell-cell communication in aquatic environments. , 2018, Current opinion in microbiology.

[29]  Rolf Backofen,et al.  Freiburg RNA tools: a central online resource for RNA-focused research and teaching , 2018, Nucleic Acids Res..

[30]  E. Charpentier,et al.  Extracellular Vesicle RNA: A Universal Mediator of Microbial Communication? , 2018, Trends in microbiology.

[31]  Thijs J. G. Ettema,et al.  Asgard archaea are the closest prokaryotic relatives of eukaryotes , 2018, PLoS genetics.

[32]  J. DiRuggiero,et al.  Transcriptional Landscape and Regulatory Roles of Small Noncoding RNAs in the Oxidative Stress Response of the Haloarchaeon Haloferax volcanii , 2018, Journal of bacteriology.

[33]  Lukas Zimmermann,et al.  A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core. , 2017, Journal of molecular biology.

[34]  M. Fürthauer,et al.  Biogenesis and function of ESCRT-dependent extracellular vesicles. , 2017, Seminars in cell & developmental biology.

[35]  R. Cavicchioli,et al.  A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells , 2017, Nature Microbiology.

[36]  Thomas K. F. Wong,et al.  ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates , 2017, Nature Methods.

[37]  M. Ohkuma,et al.  Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells , 2017, Front. Microbiol..

[38]  Thijs J. G. Ettema,et al.  Asgard archaea illuminate the origin of eukaryotic cellular complexity , 2017, Nature.

[39]  N. Popitsch,et al.  In vivo expression technology and 5′ end mapping of the Borrelia burgdorferi transcriptome identify novel RNAs expressed during mammalian infection , 2016, Nucleic acids research.

[40]  Rebecca Gamble-Milner Genetic analysis of the Hel308 helicase in the archaeon Haloferax volcanii , 2016 .

[41]  P. Jose,et al.  Functional transferred DNA within extracellular vesicles. , 2016, Experimental cell research.

[42]  D. Valentine,et al.  Important roles for membrane lipids in haloarchaeal bioenergetics. , 2016, Biochimica et biophysica acta.

[43]  Katja Koeppen,et al.  A Novel Mechanism of Host-Pathogen Interaction through sRNA in Bacterial Outer Membrane Vesicles , 2016, PLoS pathogens.

[44]  Arndt von Haeseler,et al.  W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis , 2016, Nucleic Acids Res..

[45]  M. Toyofuku,et al.  Bacterial membrane vesicles, an overlooked environmental colloid: Biology, environmental perspectives and applications. , 2015, Advances in colloid and interface science.

[46]  Y. Tashiro,et al.  Complexities of cell-to-cell communication through membrane vesicles: implications for selective interaction of membrane vesicles with microbial cells , 2015, Front. Microbiol..

[47]  Michael J E Sternberg,et al.  The Phyre2 web portal for protein modeling, prediction and analysis , 2015, Nature Protocols.

[48]  E. Yang,et al.  Extracellular Vesicles of the Hyperthermophilic Archaeon “Thermococcus onnurineus” NA1T , 2015, Applied and Environmental Microbiology.

[49]  N. Baliga,et al.  Sense overlapping transcripts in IS1341-type transposase genes are functional non-coding RNAs in archaea , 2015, RNA biology.

[50]  Yang Zhang,et al.  The I-TASSER Suite: protein structure and function prediction , 2014, Nature Methods.

[51]  Mark C. Field,et al.  Missing pieces of an ancient puzzle: evolution of the eukaryotic membrane-trafficking system. , 2014, Cold Spring Harbor perspectives in biology.

[52]  S. Chisholm,et al.  Bacterial Vesicles in Marine Ecosystems , 2014, Science.

[53]  K. Hinrichs,et al.  Application of two new LC–ESI–MS methods for improved detection of intact polar lipids (IPLs) in environmental samples , 2013 .

[54]  P. Forterre,et al.  Hyperthermophilic archaea produce membrane vesicles that can transfer DNA. , 2013, Environmental microbiology reports.

[55]  T. Allers,et al.  DNA damage induces nucleoid compaction via the Mre11-Rad50 complex in the archaeon Haloferax volcanii , 2012, Molecular microbiology.

[56]  K. Freeman,et al.  Molecular characterization of core lipids from halophilic archaea grown under different salinity conditions , 2012 .

[57]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[58]  P. Stadler,et al.  LocARNA-P: accurate boundary prediction and improved detection of structural RNAs. , 2012, RNA.

[59]  B. Cookson,et al.  Membrane Vesicle Release in Bacteria, Eukaryotes, and Archaea: a Conserved yet Underappreciated Aspect of Microbial Life , 2012, Infection and Immunity.

[60]  K. Hinrichs,et al.  Systematic fragmentation patterns of archaeal intact polar lipids by high-performance liquid chromatography/electrospray ionization ion-trap mass spectrometry. , 2011, Rapid communications in mass spectrometry : RCM.

[61]  M. Kuehn,et al.  Contribution of bacterial outer membrane vesicles to innate bacterial defense , 2011, BMC Microbiology.

[62]  Lothar Willmitzer,et al.  Elemental formula annotation of polar and lipophilic metabolites using (13) C, (15) N and (34) S isotope labelling, in combination with high-resolution mass spectrometry. , 2011, The Plant journal : for cell and molecular biology.

[63]  E. Sztul,et al.  COPII and COPI traffic at the ER-Golgi interface. , 2011, Physiology.

[64]  Scott D Emr,et al.  The ESCRT pathway. , 2011, Developmental cell.

[65]  A. Marchfelder,et al.  Bioinformatic prediction and experimental verification of sRNAs in the haloarchaeon Haloferax volcanii , 2011, RNA biology.

[66]  Hadley Wickham,et al.  The Split-Apply-Combine Strategy for Data Analysis , 2011 .

[67]  Cedric E. Ginestet ggplot2: Elegant Graphics for Data Analysis , 2011 .

[68]  E. Koonin,et al.  Evolution of diverse cell division and vesicle formation systems in Archaea , 2010, Nature Reviews Microbiology.

[69]  Paramvir S. Dehal,et al.  FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments , 2010, PloS one.

[70]  S. Liddell,et al.  Improved Strains and Plasmid Vectors for Conditional Overexpression of His-Tagged Proteins in Haloferax volcanii , 2010, Applied and Environmental Microbiology.

[71]  V. Hsu,et al.  Mechanisms of COPI vesicle formation , 2009, FEBS letters.

[72]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[73]  W. Dowhan,et al.  Cardiolipin membrane domains in prokaryotes and eukaryotes. , 2009, Biochimica et biophysica acta.

[74]  H. Stenmark Rab GTPases as coordinators of vesicle traffic , 2009, Nature Reviews Molecular Cell Biology.

[75]  H. Schwarz,et al.  Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components , 2008, Extremophiles.

[76]  O. Medalia,et al.  Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer. , 2007, Journal of molecular biology.

[77]  Rolf Backofen,et al.  Inferring Noncoding RNA Families and Classes by Means of Genome-Scale Structure-Based Clustering , 2007, PLoS Comput. Biol..

[78]  M. Kuehn,et al.  Outer Membrane Vesicle Production by Escherichia coli Is Independent of Membrane Instability , 2006, Journal of bacteriology.

[79]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[80]  R. G. Lloyd,et al.  Development of Additional Selectable Markers for the Halophilic Archaeon Haloferax volcanii Based on the leuB and trpA Genes , 2004, Applied and Environmental Microbiology.

[81]  J. Brisson,et al.  Novel polar lipids of halophilic eubacterium Planococcus H8 and archaeon Haloferax volcanii. , 2003, Biochimica et biophysica acta.

[82]  R. Ortenberg,et al.  Development of a Gene Knockout System for the Halophilic Archaeon Haloferax volcanii by Use of the pyrE Gene , 2003, Journal of bacteriology.

[83]  T. Kirchhausen,et al.  Three ways to make a vesicle , 2000, Nature Reviews Molecular Cell Biology.

[84]  S. Nickell,et al.  Sulfolobicins, Specific Proteinaceous Toxins Produced by Strains of the Extremely Thermophilic Archaeal GenusSulfolobus , 2000, Journal of bacteriology.

[85]  R. Lloubès,et al.  Escherichia coli tol-pal Mutants Form Outer Membrane Vesicles , 1998, Journal of bacteriology.

[86]  W. Lubitz,et al.  Characterization of Natronobacterium magadii phage ΦCh1, a unique archaeal phage containing DNA and RNA , 1997, Molecular microbiology.

[87]  Charles Elkan,et al.  Fitting a Mixture Model By Expectation Maximization To Discover Motifs In Biopolymer , 1994, ISMB.

[88]  W. Doolittle,et al.  Shuttle vectors for the archaebacterium Halobacterium volcanii. , 1989, Proceedings of the National Academy of Sciences of the United States of America.