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8. Whole‐genome comparison between the type strain of Halobacterium salinarum (DSM 3754T) and the laboratory strains R1 and NRC‐1

Author

Pfeiffer, Friedhelm, Losensky, Gerald, Marchfelder, Anita, Habermann, Bianca, Dyall‐Smith, Mike, Pfeiffer, Friedhelm, Losensky, Gerald, Marchfelder, Anita, Habermann, Bianca, and Dyall‐Smith, Mike

Abstract

Halobacterium salinarum is an extremely halophilic archaeon that is widely distributed in hypersaline environments and was originally isolated as a spoilage organism of salted fish and hides. The type strain 91‐R6 (DSM 3754T) has seldom been studied and its genome sequence has only recently been determined by our group. The exact relationship between the type strain and two widely used model strains, NRC‐1 and R1, has not been described before. The genome of Hbt. salinarum strain 91‐R6 consists of a chromosome (2.17 Mb) and two large plasmids (148 and 102 kb, with 39,230 bp being duplicated). Cytosine residues are methylated (m4C) within CTAG motifs. The genomes of type and laboratory strains are closely related, their chromosomes sharing average nucleotide identity (ANIb) values of 98% and in silico DNA–DNA hybridization (DDH) values of 95%. The chromosomes are completely colinear, do not show genome rearrangement, and matching segments show <1% sequence difference. Among the strain‐specific sequences are three large chromosomal replacement regions (>10 kb). The well‐studied AT‐rich island (61 kb) of the laboratory strains is replaced by a distinct AT‐rich sequence (47 kb) in 91‐R6. Another large replacement (91‐R6: 78 kb, R1: 44 kb) codes for distinct homologs of proteins involved in motility and N‐glycosylation. Most (107 kb) of plasmid pHSAL1 (91‐R6) is very closely related to part of plasmid pHS3 (R1) and codes for essential genes (e.g. arginine‐tRNA ligase and the pyrimidine biosynthesis enzyme aspartate carbamoyltransferase). Part of pHS3 (42.5 kb total) is closely related to the largest strain‐specific sequence (164 kb) in the type strain chromosome. Genome sequencing unraveled the close relationship between the Hbt. salinarum type strain and two well‐studied laboratory strains at the DNA and protein levels. Although an independent isolate, the type strain shows a remarkably low evolutionary difference to the laboratory strains.

Published
2024

9. Iron starvation results in up-regulation of a probable Haloferax volcanii siderophore transporter.

Author

Sailer, Anna-Lena, Jevtic, Zivojin, Stoll, Britta, Wörtz, Julia, Sharma, Kundan, Urlaub, Henning, Dyall-Smith, Mike, Pfeiffer, Friedhelm, Marchfelder, Anita, and Lenz, Christof

Subjects
LIBRARY acquisitions, GROWTH disorders, MASS spectrometry, MOLECULAR docking, CELL morphology
Abstract

The response of the haloarchaeal model organism Haloferax volcanii to iron starvation was analyzed at the proteome level by data-independent acquisition mass spectrometry. Cells grown in minimal medium with normal iron levels were compared to those grown under low iron conditions, with samples being separated into membrane and cytoplasmic fractions in order to focus on import/export processes which are frequently associated with metal homeostasis. Iron starvation not only caused a severe retardation of growth but also altered the levels of many proteins. Using a comprehensive annotated spectral library and data-independent acquisition mass spectrometry (DIA-MS), we found that iron starvation resulted in significant changes to both the membrane and the soluble proteomes of Hfx. volcanii. The most affected protein is the RND family permease HVO_A0467, which is 44-fold enriched in cells grown under iron starvation. The gene HVO_A0467 can be deleted suggesting that it is not essential under standard conditions. Compared to wild type cells the deletion strain shows only slight changes in growth and cell morphologies show no differences. Molecular docking predictions indicated that HVO_A0467 may be an exporter of the siderophore schizokinen for which a potential biosynthesis cluster is encoded in the Hfx. volcanii genome. Together, these findings confirm the importance of iron for archaeal cells and suggest HVO_0467 as a siderophore exporter. [ABSTRACT FROM AUTHOR]

Published
2024
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13. The Archaeal Proteome Project advances knowledge about archaeal cell biology through comprehensive proteomics

Author

Schulze, Stefan, Adams, Zachary, Cerletti, Micaela, De Castro, Rosana, Ferreira-Cerca, Sébastien, Fufezan, Christian, Giménez, María Inés, Hippler, Michael, Jevtic, Zivojin, Knüppel, Robert, Legerme, Georgio, Lenz, Christof, Marchfelder, Anita, Maupin-Furlow, Julie, Paggi, Roberto A., Pfeiffer, Friedhelm, Poetsch, Ansgar, Urlaub, Henning, and Pohlschroder, Mechthild

Published
2020
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14. Extracellular vesicle formation in Euryarchaeota is driven by a small GTPase.

Author

Mills, Joshua, Gebhard, L. Johanna, Schubotz, Florence, Shevchenko, Anna, Speth, Daan R., Yan Liao, Duggin, Iain G., Marchfelder, Anita, and Erdmann, Susanne

Subjects
EXTRACELLULAR vesicles, GUANOSINE triphosphatase, ELECTRIC vehicle industry, HALOBACTERIUM, OPERONS, TELECOMMUNICATION systems
Abstract

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 Euryarchaeota, using the model organism Haloferax volcanii. 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 small GTPase for EV formation in H. volcanii that is also present across other diverse evolutionary branches of Archaea. We propose the name, ArvA, for the identified family of archaeal vesiculating GTPases. Additionally, we show that two genes in the same operon with arvA (arvB and arvC) are also involved in EV formation. Both, arvB and arvC, are closely associated with arvA in the majority of other archaea encoding ArvA. Our work demonstrates that small GTPases involved in membrane deformation and vesiculation, ubiquitous in Eukaryotes, are also present in Archaea and are widely distributed across diverse archaeal phyla. [ABSTRACT FROM AUTHOR]

Published
2024
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20. Identification and characterization of structural and regulatory cell-shape determinants inHaloferax volcanii

Author

Schiller, Heather, primary, Kouassi, Joshua, additional, Hong, Yirui, additional, Rados, Theopi, additional, Kwak, Jasmin, additional, DiLucido, Anthony, additional, Safer, Daniel, additional, Marchfelder, Anita, additional, Pfeiffer, Friedhelm, additional, Bisson-Filho, Alexandre, additional, Schulze, Stefan, additional, and Pohlschroder, Mechthild, additional

Published
2023
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25. An archaeal Cas3 protein facilitates rapid recovery from DNA damage

Author

Miezner, Guy, primary, Turgeman-Grott, Israela, additional, Zatopek, Kelly M, additional, Gardner, Andrew F, additional, Reshef, Leah, additional, Choudhary, Deepak K, additional, Altstetter, Martina, additional, Allers, Thorsten, additional, Marchfelder, Anita, additional, and Gophna, Uri, additional

Published
2023
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26. Revealing the small proteome ofHaloferax volcaniiby combining ribosome profiling and small-protein optimized mass spectrometry

Author

Hadjeras, Lydia, primary, Bartel, Jürgen, additional, Maier, Lisa-Katharina, additional, Maaß, Sandra, additional, Vogel, Verena, additional, Svensson, Sarah L, additional, Eggenhofer, Florian, additional, Gelhausen, Rick, additional, Müller, Teresa, additional, Alkhnbashi, Omer S, additional, Backofen, Rolf, additional, Becher, Dörte, additional, Sharma, Cynthia M, additional, and Marchfelder, Anita, additional

Published
2023
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27. A Complex of Cas Proteins 5, 6, and 7 Is Required for the Biogenesis and Stability of Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)-derived RNAs (crRNAs) in Haloferax volcanii

Author

Brendel, Jutta, Stoll, Britta, Lange, Sita J., Sharma, Kundan, Lenz, Christof, Stachler, Aris-Edda, Maier, Lisa-Katharina, Richter, Hagen, Nickel, Lisa, Schmitz, Ruth A., Randau, Lennart, Allers, Thorsten, Urlaub, Henning, Backofen, Rolf, and Marchfelder, Anita

Published
2014
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32. Cas1 and Fen1 Display Equivalent Functions During Archaeal DNA Repair

Author

Wörtz, Julia, Smith, Victoria, Fallmann, Jörg, König, Sabine, Thuraisingam, Tharani, Walther, Paul, Urlaub, Henning, Stadler, Peter F., Allers, Thorsten, Hille, Frank, and Marchfelder, Anita

Subjects
Microbiology (medical), CRISPR/Cas-Methode, CRISPR-Cas systems, Archaebakterien, DNS-Reparatur, archaea, DNA repair, Archaea, Microbiology, Cas1, ddc:570, Fen1, ddc:610, CRISPR-Cas, Haloferax volcanii
Abstract

CRISPR-Cas constitutes an adaptive prokaryotic defence system against invasive nucleic acids like viruses and plasmids. Beyond their role in immunity, CRISPR-Cas systems have been shown to closely interact with components of cellular DNA repair pathways, either by regulating their expression or via direct protein-protein contact and enzymatic activity. The integrase Cas1 is usually involved in the adaptation phase of CRISPR-Cas immunity but an additional role in cellular DNA repair pathways has been proposed previously. Here, we analysed the capacity of an archaeal Cas1 from Haloferax volcanii to act upon DNA damage induced by oxidative stress and found that a deletion of the cas1 gene led to reduced survival rates following stress induction. In addition, our results indicate that Cas1 is directly involved in DNA repair as the enzymatically active site of the protein is crucial for growth under oxidative conditions. Based on biochemical assays, we propose a mechanism by which Cas1 plays a similar function to DNA repair protein Fen1 by cleaving branched intermediate structures. The present study broadens our understanding of the functional link between CRISPR-Cas immunity and DNA repair by demonstrating that Cas1 and Fen1 display equivalent roles during archaeal DNA damage repair.

Published
2022
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36. The Archaeal Lsm Protein Binds to Small RNAs

Author

Fischer, Susan, Benz, Juliane, Späth, Bettina, Maier, Lisa-Katharina, Straub, Julia, Granzow, Michaela, Raabe, Monika, Urlaub, Henning, Hoffmann, Jan, Brutschy, Bernd, Allers, Thorsten, Soppa, Jörg, and Marchfelder, Anita

Published
2010
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38. Revealing the small proteome of Haloferax volcanii by combining ribosome profiling and small-protein optimized mass spectrometry.

Author

Hadjeras, Lydia, Bartel, Jürgen, Maier, Lisa-Katharina, Maaß, Sandra, Vogel, Verena, Svensson, Sarah L, Eggenhofer, Florian, Gelhausen, Rick, Müller, Teresa, Alkhnbashi, Omer S, Backofen, Rolf, Becher, Dörte, Sharma, Cynthia M, and Marchfelder, Anita

Abstract

In contrast to extensively studied prokaryotic 'small' transcriptomes (encompassing all small noncoding RNAs), small proteomes (here defined as including proteins ≤70 aa) are only now entering the limelight. The absence of a complete small protein catalogue in most prokaryotes precludes our understanding of how these molecules affect physiology. So far, archaeal genomes have not yet been analyzed broadly with a dedicated focus on small proteins. Here, we present a combinatorial approach, integrating experimental data from small protein-optimized mass spectrometry (MS) and ribosome profiling (Ribo-seq), to generate a high confidence inventory of small proteins in the model archaeon Haloferax volcanii. We demonstrate by MS and Ribo-seq that 67% of the 317 annotated small open reading frames (sORFs) are translated under standard growth conditions. Furthermore, annotation-independent analysis of Ribo-seq data showed ribosomal engagement for 47 novel sORFs in intergenic regions. A total of seven of these were also detected by proteomics, in addition to an eighth novel small protein solely identified by MS. We also provide independent experimental evidence in vivo for the translation of 12 sORFs (annotated and novel) using epitope tagging and western blotting, underlining the validity of our identification scheme. Several novel sORFs are conserved in Haloferax species and might have important functions. Based on our findings, we conclude that the small proteome of H. volcanii is larger than previously appreciated, and that combining MS with Ribo-seq is a powerful approach for the discovery of novel small protein coding genes in archaea. [ABSTRACT FROM AUTHOR]

Published
2023
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40. RNA Processing

Author

Klug, Gabriele, primary, Evguenieva-Hackenberg, Elena, additional, Omer, Arina D., additional, Dennis, Patrick P., additional, and Marchfelder, Anita, additional

Published
2014
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42. A Small RNA Is Linking CRISPR–Cas and Zinc Transport

Author

Märkle, Pascal, Maier, Lisa-Katharina, Maaß, Sandra, Hirschfeld, Claudia, Bartel, Jürgen, Becher, Dörte, Voß, Björn, and Marchfelder, Anita

Subjects
Archaebakterien, QH301-705.5, Archaebacteria, Archaea, Small RNA, zinc transport, DDC 570 / Life sciences, ddc:570, RNA, Small Untranslated, Molecular Biosciences, Biology (General), CRISPR-Cas, CRISPR-Cas Systems, Non-coding RNA, haloarchaea, Original Research
Abstract

The function and mode of action of small regulatory RNAs is currently still understudied in archaea. In the halophilic archaeon Haloferax volcanii, a plethora of sRNAs have been identified; however, in-depth functional analysis is missing for most of them. We selected a small RNA (s479) from Haloferax volcanii for detailed characterization. The sRNA gene is encoded between a CRISPR RNA locus and the Cas protein gene cluster, and the s479 deletion strain is viable and was characterized in detail. Transcriptome studies of wild-type Haloferax cells and the deletion mutant revealed upregulation of six genes in the deletion strain, showing that this sRNA has a clearly defined function. Three of the six upregulated genes encode potential zinc transporter proteins (ZnuA1, ZnuB1, and ZnuC1) suggesting the involvement of s479 in the regulation of zinc transport. Upregulation of these genes in the deletion strain was confirmed by northern blot and proteome analyses. Furthermore, electrophoretic mobility shift assays demonstrate a direct interaction of s479 with the target znuC1 mRNA. Proteome comparison of wild-type and deletion strains further expanded the regulon of s479 deeply rooting this sRNA within the metabolism of H. volcanii especially the regulation of transporter abundance. Interestingly, s479 is not only encoded next to CRISPR���cas genes, but the mature s479 contains a crRNA-like 5��� handle, and experiments with Cas protein deletion strains indicate maturation by Cas6 and interaction with Cas proteins. Together, this might suggest that the CRISPR���Cas system is involved in s479 function., publishedVersion

Published
2021

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