Understanding the Adaptation of <i>Halobacterium</i> Species NRC-1 to Its Extreme Environment through Computational Analysis of Its Genome Sequence

Kennedy, Sean P.; Ng, Wailap Victor; Salzberg, Steven L.; Hood, Leroy; DasSarma, Shiladitya

doi:10.1101/gr.190201

Cited by 301 publications

(280 citation statements)

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“…As an example we highlight the cydA gene, which encodes for the cytochrome bd ubiquinol oxidase subunit I, and was probably acquired from bacteria along with other aerobic respiration genes [69]. We found that in E. coli this gene presents an iTSS (TSS_873, locus b0733) for a putative intraRNA that, if translated using the first available ATG start codon 29 nt downstream, would produce a 43.9 kDa isoform of the 58.2 kDa CydA cognate protein.…”

Section: Resultsmentioning

confidence: 99%

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

et al. 2018

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Prokaryotic genomes show a high level of information compaction often with different molecules transcribed from the same locus. Although antisense RNAs have been relatively well studied, RNAs in the same strand, internal RNAs (intraRNAs), are still poorly understood. The question of how common is the translation of overlapping reading frames remains open. We address this question in the model archaeon Halobacterium salinarum. In the present work we used differential RNA-seq (dRNA-seq) in H. salinarum NRC-1 to locate intraRNA signals in subsets of internal transcription start sites (iTSS) and establish the open reading frames associated to them (intraORFs). Using C-terminally flagged proteins, we experimentally observed isoforms accurately predicted by intraRNA translation for kef1, acs3 and orc4 genes. We also recovered from the literature and mass spectrometry databases several instances of protein isoforms consistent with intraRNA translation such as the gas vesicle protein gene gvpC1. We found evidence for intraRNAs in horizontally transferred genes such as the chaperone dnaK and the aerobic respiration related cydA in both H. salinarum and Escherichia coli. Also, intraRNA translation evidence in H. salinarum, E. coli and yeast of a universal elongation factor (aEF-2, fusA and eEF-2) suggests that this is an ancient phenomenon present in all domains of life.

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Section: Resultsmentioning

confidence: 99%

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

et al. 2018

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“…It is commonly anticipated that the ancestor of this highly specialized group was a strictly anaerobic, chemolithoautotrophic methanogen. Its transformation to haloarchaea, which we know today required a lateral gene transfer on a massive scale (Kennedy et al, 2001;Khomyakova et al, 2011;Nelson-Sathi et al, 2012. Therefore, haloarchaeal metabolism combines mostly laterally transferred, aerobic heterotrophic pathways from Bacteria, with some vertically inherited features of the methanogenic ancestor.…”

Section: Introductionmentioning

confidence: 99%

The methylaspartate cycle in haloarchaea and its possible role in carbon metabolism

et al. 2015

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Haloarchaea (class Halobacteria) live in extremely halophilic conditions and evolved many unique metabolic features, which help them to adapt to their environment. The methylaspartate cycle, an anaplerotic acetate assimilation pathway recently proposed for Haloarcula marismortui, is one of these special adaptations. In this cycle, acetyl-CoA is oxidized to glyoxylate via methylaspartate as a characteristic intermediate. The following glyoxylate condensation with another molecule of acetylCoA yields malate, a starting substrate for anabolism. The proposal of the functioning of the cycle was based mainly on in vitro data, leaving several open questions concerning the enzymology involved and the occurrence of the cycle in halophilic archaea. Using gene deletion mutants of H. hispanica, enzyme assays and metabolite analysis, we now close these gaps by unambiguous identification of the genes encoding all characteristic enzymes of the cycle. Based on these results, we were able to perform a solid study of the distribution of the methylaspartate cycle and the alternative acetate assimilation strategy, the glyoxylate cycle, among haloarchaea. We found that both of these cycles are evenly distributed in haloarchaea. Interestingly, 83% of the species using the methylaspartate cycle possess also the genes for polyhydroxyalkanoate biosynthesis, whereas only 34% of the species with the glyoxylate cycle are capable to synthesize this storage compound. This finding suggests that the methylaspartate cycle is shaped for polyhydroxyalkanoate utilization during carbon starvation, whereas the glyoxylate cycle is probably adapted for growth on substrates metabolized via acetyl-CoA.

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“…Halobacterium NRC-1, for example, has evolved the capacity to withstand up to 4.5M salinity, ultraviolet radiation (UV), and oxidative stress in its natural environment. One such adaptation, the high-density of acidic residues on the surface of almost all halobacterial proteins, is believed to stabilize protein structure and function in high salt (Kennedy et al 2001). It can also physically relocate to favorable environments using sensors for light, oxygen, and nutrients, and produce energy through respiration, fermentation, or phototrophy (Ng et al 2000).…”

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Systems Level Insights Into the Stress Response to UV Radiation in the Halophilic ArchaeonHalobacterium NRC-1

Baliga¹,

Bjork²,

Bonneau³

et al. 2004

Genome Res.

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We report a remarkably high UV-radiation resistance in the extremely halophilic archaeon Halobacterium NRC-1 withstanding up to 110 J/m 2 with no loss of viability. Gene knockout analysis in two putative photolyase-like genes (phr1 and phr2) implicated only phr2 in photoreactivation. The UV-response was further characterized by analyzing simultaneously, along with gene function and protein interactions inferred through comparative genomics approaches, mRNA changes for all 2400 genes during light and dark repair. In addition to photoreactivation, three other putative repair mechanisms were identified including d(CTAG) methylation-directed mismatch repair, four oxidative damage repair enzymes, and two proteases for eliminating damaged proteins. Moreover, a UV-induced down-regulation of many important metabolic functions was observed during light repair and seems to be a phenomenon shared by all three domains of life. The systems analysis has facilitated the assignment of putative functions to 26 of 33 key proteins in the UV response through sequence-based methods and/or similarities of their predicted three-dimensional structures to known structures in the PDB. Finally, the systems analysis has raised, through the integration of experimentally determined and computationally inferred data, many experimentally testable hypotheses that describe the metabolic and regulatory networks of Halobacterium NRC-1.[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GEO under accession no. GSE1040.]Biological systems have evolved mechanisms to appropriately respond to environmental stresses that can damage proteins and DNA. Halobacterium NRC-1, for example, has evolved the capacity to withstand up to 4.5M salinity, ultraviolet radiation (UV), and oxidative stress in its natural environment. One such adaptation, the high-density of acidic residues on the surface of almost all halobacterial proteins, is believed to stabilize protein structure and function in high salt (Kennedy et al. 2001). It can also physically relocate to favorable environments using sensors for light, oxygen, and nutrients, and produce energy through respiration, fermentation, or phototrophy (Ng et al. 2000). We have previously reported a response mechanism in Halobacterium NRC-1 that coordinately regulates phototrophy and arginine fermentation, two major sources for anaerobic energy production. The effects of perturbing the function of a regulator in this response mechanism were observed throughout the metabolic network (Baliga et al. 2002).Systems approaches allow us to raise a whole series of hypotheses regarding the behavior of a system in response to a defined experimental perturbation. These hypotheses then stimulate iterative cycles of perturbations and analyses to verify these hypotheses. Here, we report a systems-level study on the behavior of Halobacterium NRC-1 upon UV-C irradiation. Shortwave ultraviolet light (UV-C) induces two types of mutagenic lesions in DNA-cyclobutane pyrimid...

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Understanding the Adaptation of Halobacterium Species NRC-1 to Its Extreme Environment through Computational Analysis of Its Genome Sequence

Cited by 301 publications

References 51 publications

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

The methylaspartate cycle in haloarchaea and its possible role in carbon metabolism

Systems Level Insights Into the Stress Response to UV Radiation in the Halophilic ArchaeonHalobacterium NRC-1

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