The Genome Sequence of the Halobacterium salinarum Type Strain Is Closely Related to That of Laboratory Strains NRC-1 and R1

Pfeiffer, Friedhelm; Marchfelder, Anita; Habermann, Bianca; Dyall‐Smith, Mike

doi:10.1128/mra.00429-19

Cited by 11 publications

(14 citation statements)

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“…A small number of positions differed from that of the reference. Some of these differences are consistent with those of later sequence reports (Pfeiffer et al, 2008(Pfeiffer et al, , 2019. The sequences differences shown in Supplementary Table S4 were excluded in our analysis of the evolved clones.…”

Section: Mutations In the Genomes From Evolving Populationssupporting

confidence: 82%

Acid Experimental Evolution of the Haloarchaeon Halobacterium sp. NRC-1 Selects Mutations Affecting Arginine Transport and Catabolism

et al. 2020

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Halobacterium sp. NRC-1 (NRC-1) is an extremely halophilic archaeon that is adapted to multiple stressors such as UV, ionizing radiation and arsenic exposure; it is considered a model organism for the feasibility of microbial life in iron-rich brine on Mars. We conducted experimental evolution of NRC-1 under acid and iron stress. NRC-1 was serially cultured in CM + medium modified by four conditions: optimal pH (pH 7.5), acid stress (pH 6.3), iron amendment (600 µM ferrous sulfate, pH 7.5), and acid plus iron (pH 6.3, with 600 µM ferrous sulfate). For each condition, four independent lineages of evolving populations were propagated. After 500 generations, 16 clones were isolated for phenotypic characterization and genomic sequencing. Genome sequences of all 16 clones revealed 378 mutations, of which 90% were haloarchaeal insertion sequences (ISH) and ISH-mediated large deletions. This proportion of ISH events in NRC-1 was five-fold greater than that reported for comparable evolution of Escherichia coli. One acid-evolved clone had increased fitness compared to the ancestral strain when cultured at low pH. Seven of eight acid-evolved clones had a mutation within or upstream of arcD, which encodes an arginine-ornithine antiporter; no non-acid adapted strains had arcD mutations. Mutations also affected the arcR regulator of arginine catabolism, which protects bacteria from acid stress by release of ammonia. Two acid-adapted strains shared a common mutation in bop, which encodes bacterio-opsin, apoprotein for the bacteriorhodopsin light-driven proton pump. Thus, in the haloarchaeon NRC-1, as in bacteria, pH adaptation was associated with genes involved in arginine catabolism and proton transport. Our study is among the first to report experimental evolution with multiple resequenced genomes of an archaeon. Haloarchaea are polyextremophiles capable of growth under environmental conditions such as concentrated NaCl and desiccation, but little is known about pH stress. Interesting parallels appear between the molecular basis of pH adaptation in NRC-1 and in bacteria, particularly the acid-responsive arginine-ornithine system found in oral streptococci.

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Section: Mutations In the Genomes From Evolving Populationssupporting

confidence: 82%

Acid Experimental Evolution of the Haloarchaeon Halobacterium sp. NRC-1 Selects Mutations Affecting Arginine Transport and Catabolism

et al. 2020

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“…After validation, the cell pellet was sent to the Max‐Planck Genome Center Cologne (https://www.mpgc.mpipz.mpg.de) for DNA extraction, library preparation, and sequencing as reported previously (Pfeiffer et al, ). The sequence was determined with a PacBio RSII instrument (Rhoads & Au, ).…”

Section: Methodsmentioning

confidence: 99%

“…As reported previously (Pfeiffer et al, ), an initial and automated genome assembly was performed at the Max‐Planck Genome Center Cologne, using the SMRTanalysis pipeline (PacificBiosciences) which runs HGAP (DAGCON‐based hierarchical genome assembly process, RS_HGAP_assembly.2 version 2.3.0) with the following three steps: preassembly, de novo assembly with the Celera assembler and final polishing with Quiver. The data originated from five SMRT cells.…”

Section: Methodsmentioning

confidence: 99%

“…We have determined the complete genome sequence of the type strain of Hbt. salinarum (strain 91‐R6; DSM 3754 T ) using long‐read PacBio sequencing (Pfeiffer, Marchfelder, Habermann, & Dyall‐Smith, ). Here we describe its characteristics in more detail and then focus on its relationship to the widely studied laboratory strains R1 and NRC‐1 at the DNA and protein levels.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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 3754 T ) 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 ( m4 C) 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. K E Y W O R D Scomparative genomics, genomic variability, haloarchaea, halobacteria, megaplasmid, type strain 2 of 44 | PFEIFFER Et al.

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“…However, we used a biologically relevant variation that we have used previously for Natronomonas moolapensis (Dyall-Smith et al, 2013), Halobacterium hubeiense (Jaakkola et al, 2016) and Hbt. salinarum strain 91-R6 T (Pfeiffer et al, 2019(Pfeiffer et al, , 2020.…”

Section: Hfx Gibbonsii Lr2-5 Has a Main Chromosome And Three Plasmidsmentioning

confidence: 99%

Cellular and genomic properties ofHaloferax gibbonsiiLR2-5, the host of euryarchaeal virus HFTV1

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et al. 2020

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Hypersaline environments are the source of many viruses infecting different species of halophilic euryarchaea. Information on infection mechanisms of archaeal viruses is scarce, due to the lack of genetically accessible virus-host models. Recently a new archaeal siphovirus, Haloferax tailed virus 1 (HFTV1), was isolated together with its host belonging to the genus Haloferax, but it is not infectious on the widely used model euryarcheon Hfx. volcanii. To gain more insight into the biology of HFTV1 host strain LR2-5, we studied characteristics that might play a role in its virus susceptibility: growth-dependent motility, surface layer, filamentous surface structures and cell shape. Its genome sequence showed that LR2-5 is a new strain of Hfx. gibbonsii. LR2-5 lacks obvious viral defense systems, such as CRISPR-Cas, and the composition of its cell surface is different from Hfx. volcanii, which might explain the different viral host range. This work provides first deep insights into the relationship between the host of halovirus HFTV1 and other members of the genus Haloferax. Given the close relationship to the genetically accessible Hfx. volcanii, LR2-5 has high potential as a new model for virus-host studies in euryarchaea.

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The Genome Sequence of the Halobacterium salinarum Type Strain Is Closely Related to That of Laboratory Strains NRC-1 and R1

Cited by 11 publications

References 10 publications

Acid Experimental Evolution of the Haloarchaeon Halobacterium sp. NRC-1 Selects Mutations Affecting Arginine Transport and Catabolism

Acid Experimental Evolution of the Haloarchaeon Halobacterium sp. NRC-1 Selects Mutations Affecting Arginine Transport and Catabolism

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

Cellular and genomic properties ofHaloferax gibbonsiiLR2-5, the host of euryarchaeal virus HFTV1

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The Genome Sequence of the Halobacterium salinarum Type Strain Is Closely Related to That of Laboratory Strains NRC-1 and R1

Cited by 11 publications

References 10 publications

Acid Experimental Evolution of the Haloarchaeon Halobacterium sp. NRC-1 Selects Mutations Affecting Arginine Transport and Catabolism

Acid Experimental Evolution of the Haloarchaeon Halobacterium sp. NRC-1 Selects Mutations Affecting Arginine Transport and Catabolism

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

Cellular and genomic properties ofHaloferax gibbonsiiLR2-5, the host of euryarchaeal virus HFTV1

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