Stringent control in the archaeal genus Sulfolobus

Cellini, Andrea; Scoarughi, Gian Luca; Poggiali, Paola; Santino, Iolanda; Sessa, Rosa; Donini, Pierluigi; Cimmino, Carmen

doi:10.1016/j.resmic.2003.11.006

Cited by 21 publications

(18 citation statements)

References 36 publications

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“…In Bacteria and Archaea, the levels of ribosomes vary with growth conditions (31,32). We speculate that, under famine conditions or during stringent control (33), when ribosome synthesis is likely to be decreased, a/eIF2-␥ counteracts 5Ј-to-3Ј mRNA decay. Preliminary experiments designed to mimic feast and famine conditions seem to be in line with this hypothesis.…”

Section: Discussionmentioning

confidence: 93%

Translation initiation factor a/eIF2(-γ) counteracts 5′ to 3′ mRNA decay in the archaeon Sulfolobus solfataricus

Hasenöhrl

Lombo

Kaberdin

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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The trimeric translation initiation factor a/eIF2 of the crenarchaeon Sulfolobus solfataricus is pivotal for binding of initiator tRNA to the ribosome. Here, we present in vitro and in vivo evidence that the a/eIF2 ␥-subunit exhibits an additional function with resemblance to the eukaryotic cap-complex. It binds to the 5-triphosphate end of mRNA and protects the 5 part from degradation. This unprecedented capacity of the archaeal initiation factor further indicates that 5 3 3 directional mRNA decay is a pathway common to all domains of life. In Escherichia coli, the decay of most RNA transcripts appears to be initiated by 5Ј pyrophosphate removal (1), followed by endonucleolytic cleavages that are generated by RNase E (2, 3). The intermediate cleavage products are further degraded by the 3Ј 3 5Ј exonucleases polynucleotide phosphorylase (PNPase), RNase II, and oligoribonuclease, converting the decay intermediates into poly-and mononucleotides (4). At variance with E. coli, Bacillus subtilis possesses a 5Ј 3 3Ј exonuclease activity, which could explain why RNAs in this organism are stabilized for great distances downstream of stable secondary structures or bound ribosomes (5). In eukaryotes, mRNA decay is mainly catalyzed by exonucleases (6). Eukaryotic mRNAs generally have a 7-methylguanosine cap at their 5Ј end and a poly(A) tail at their 3Ј end. Removal of these terminal modifications is considered rate-limiting for mRNA decay (7). Translation initiation factor eIF4E binds to the 7-methylguanosine cap and thereby protects the cap structure from the decapping enzyme and consequently the mRNA from 5Ј 3 3Ј exonucleolytic decay (7). Different RNases with either endo-or exonuclease activity (8-11) have been inferred or described in Archaea. In S. solfataricus a 3Ј 3 5Ј directional decay by a multisubunit exosome complex has been demonstrated in vitro (10). In addition, the Sulfolobus solfataricus exosome is able to polyadenylate the 3Ј end of RNAs in the presence of ADP (12). With the exception of the exosome, no other endo-or exonuclease activities have been described in S. solfataricus. At variance with a previous study wherein the longevity of selected S. solfataricus mRNAs was found to be rather high (13), a recent microarraybased analysis (14) indicated a rather short mRNA half-life, comparable with that of bacterial mRNAs.Two different mechanisms for translational initiation seem to exist in Sulfolobus (15). One is based on a canonical SD/anti-SD interaction and operates on internal cistrons of polycistronic mRNAs. In contrast, monocistronic mRNAs and proximal genes of polycistronic mRNAs are frequently devoid of a 5Ј untranslated region. Decoding of these leaderless mRNAs requires, analogously to Bacteria (16), pairing of the start codon with initiator-tRNA (15). The complexity of archaeal translational initiation seems to be underscored by the presence of a largerthan-bacterial set of factors because Archaea encode Ϸ10 orthologs of eukaryal and bacterial initiation factors (17). Like its eukaryotic counterp...

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Section: Discussionmentioning

confidence: 93%

Translation initiation factor a/eIF2(-γ) counteracts 5′ to 3′ mRNA decay in the archaeon Sulfolobus solfataricus

Hasenöhrl

Lombo

Kaberdin

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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“…In archaea, both relaxed and stringent strains have been observed (3,5,26). In addition, leucine limitation decreased mRNA levels for genes of methanogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…An example of a pathway-specific response is found in the regulation of the trp operon by tryptophan in Methanothermobacter thermautotrophicus, mediated by the TrpY repressor (12,34). On the global level, a subset of archaeal species possesses a stringent response; however, they do not employ the guanosine tetra-and pentaphosphates characteristic of bacterial systems, and the mechanism of stringency in archaea remains unknown (3,5,26).…”

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confidence: 99%

Global Responses of Methanococcus maripaludis to Specific Nutrient Limitations and Growth Rate

et al. 2008

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Continuous culture, transcriptome arrays, and measurements of cellular amino acid pools and tRNA charging levels were used to determine the response of Methanococcus maripaludis to leucine limitation. For comparison, the responses to phosphate and H 2 limitations were measured as well. In addition, the effect of growth rate was determined. Leucine limitation resulted in a broad response. tRNA Leu charging decreased, but only small increases in mRNA were seen for amino acid biosynthesis genes. However, the cellular levels of free isoleucine and valine showed significant increases, indicating a coordinate regulation of branched-chain amino acids at a post-mRNA level. Leucine limitation also resulted in increased mRNA abundance for ribosomal protein genes, increased rRNA abundance, and decreased mRNA abundance for genes of methanogenesis. In contrast, phosphate limitation induced a specific response, a marked increase in mRNA levels for a phosphate transporter. Some mRNA levels responded to more than one factor; for example, transcripts for flagellum synthesis genes decreased under conditions of leucine limitation and increased under H 2 limitation. Increased growth rate resulted in increased mRNA levels for ribosomal protein genes, increased rRNA abundance, and increased mRNA for a gene encoding an S-layer protein.

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“…This coupling allows bacterial cells to quickly redirect the cellular metabolism during the stringent response. The stringent response in archaea apparently differs from that in bacteria, as in Sulfolobus it is not linked to decreasing GTP concentrations (7), and the bacterial alarmone ppGpp is probably generally absent in archaea (7,32). An important question is how archaea link ribosome biogenesis with the energy state of the cell.…”

Section: Vol 193 2011mentioning

confidence: 99%

An HflX-Type GTPase from Sulfolobus solfataricus Binds to the 50S Ribosomal Subunit in All Nucleotide-Bound States

et al. 2011

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HflX GTPases are found in all three domains of life, the Bacteria, Archaea, and Eukarya. HflX from Escherichia coli has been shown to bind to the 50S ribosomal subunit in a nucleotide-dependent manner, and this interaction strongly stimulates its GTPase activity. We recently determined the structure of an HflX ortholog from the archaeon Sulfolobus solfataricus (SsoHflX). It revealed the presence of a novel HflX domain that might function in RNA binding and is linked to a canonical G domain. This domain arrangement is common to all archaeal, bacterial, and eukaryotic HflX GTPases. This paper shows that the archaeal SsoHflX, like its bacterial orthologs, binds to the 50S ribosomal subunit. This interaction does not depend on the presence of guanine nucleotides. The HflX domain is sufficient for ribosome interaction. Binding appears to be restricted to free 50S ribosomal subunits and does not occur with 70S ribosomes engaged in translation. The fingerprint 1 H-15 N heteronuclear correlation nuclear magnetic resonance (NMR) spectrum of SsoHflX reveals a large number of well-resolved resonances that are broadened upon binding to the 50S ribosomal subunit. The GTPase activity of SsoHflX is stimulated by crude fractions of 50S ribosomal subunits, but this effect is lost with further high-salt purification of the 50S ribosomal subunits, suggesting that the stimulation depends on an extrinsic factor bound to the 50S ribosomal subunit. Our results reveal common properties but also marked differences between archaeal and bacterial HflX proteins.

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Stringent control in the archaeal genus Sulfolobus

Cited by 21 publications

References 36 publications

Translation initiation factor a/eIF2(-γ) counteracts 5′ to 3′ mRNA decay in the archaeon Sulfolobus solfataricus

Translation initiation factor a/eIF2(-γ) counteracts 5′ to 3′ mRNA decay in the archaeon Sulfolobus solfataricus

Global Responses of Methanococcus maripaludis to Specific Nutrient Limitations and Growth Rate

An HflX-Type GTPase from Sulfolobus solfataricus Binds to the 50S Ribosomal Subunit in All Nucleotide-Bound States

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