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Rnomics and Modomics in the Halophilic Archaea Haloferax Volcanii: Identification of RNA Modification Genes

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RNomics and Modomics in the halophilic archaea Haloferax volcanii: identification of RNA modification genes. Henri Grosjean, Christine Gaspin, Christian Marck, Wayne A Decatur, Valérie de Crécy-Lagard To cite this version: Henri Grosjean, Christine Gaspin, Christian Marck, Wayne A Decatur, Valérie de Crécy-Lagard. RNomics and Modomics in the halophilic archaea Haloferax volcanii: identification of RNA modifi- cation genes.. BMC Genomics, BioMed Central, 2008, 9, pp.470. 10.1186/1471-2164-9-470. hal- 00354522 HAL Id: hal-00354522 https://hal.archives-ouvertes.fr/hal-00354522 Submitted on 31 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. BMC Genomics BioMed Central Research article Open Access RNomics and Modomics in the halophilic archaea Haloferax volcanii: identification of RNA modification genes Henri Grosjean1,2,3, Christine Gaspin4, Christian Marck5, Wayne A Decatur6 and Valérie de Crécy-Lagard*1 Address: 1Department of Microbiology and Department of Microbiology and Cell Science, University of Florida, Gainsville, FL-32611, Florida, USA, 2IGM, Université de Paris-sud, UMR 8621, Orsay, F 91405, France, 3CNRS, IGM, Orsay, F-91405, France, 4National Institute of Agronomical Research, Biometrics and Artificial Intelligence Department, Chemin de Borde-Rouge, Auzeville BP 27, 31326 Castanet-Tolosan, France, 5Institut de Biologie et de Technologies de Saclay (iBiTecS), Commissariat à l'Energie Atomique (CEA), Gif sur Yvette, F-91191, France and 6Department of Biochemistry and Molecular Biology, University of Massachussets, Amerherst, MA 01003, Massachusetts, USA Email: Henri Grosjean - [email protected]; Christine Gaspin - [email protected]; Christian Marck - [email protected]; Wayne A Decatur - [email protected]; Valérie de Crécy-Lagard* - [email protected] * Corresponding author Published: 9 October 2008 Received: 1 July 2008 Accepted: 9 October 2008 BMC Genomics 2008, 9:470 doi:10.1186/1471-2164-9-470 This article is available from: http://www.biomedcentral.com/1471-2164/9/470 © 2008 Grosjean et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Naturally occurring RNAs contain numerous enzymatically altered nucleosides. Differences in RNA populations (RNomics) and pattern of RNA modifications (Modomics) depends on the organism analyzed and are two of the criteria that distinguish the three kingdoms of life. If the genomic sequences of the RNA molecules can be derived from whole genome sequence information, the modification profile cannot and requires or direct sequencing of the RNAs or predictive methods base on the presence or absence of the modifications genes. Results: By employing a comparative genomics approach, we predicted almost all of the genes coding for the t+rRNA modification enzymes in the mesophilic moderate halophile Haloferax volcanii. These encode both guide RNAs and enzymes. Some are orthologous to previously identified genes in Archaea, Bacteria or in Saccharomyces cerevisiae, but several are original predictions. Conclusion: The number of modifications in t+rRNAs in the halophilic archaeon is surprisingly low when compared with other Archaea or Bacteria, particularly the hyperthermophilic organisms. This may result from the specific lifestyle of halophiles that require high intracellular salt concentration for survival. This salt content could allow RNA to maintain its functional structural integrity with fewer modifications. We predict that the few modifications present must be particularly important for decoding, accuracy of translation or are modifications that cannot be functionally replaced by the electrostatic interactions provided by the surrounding salt-ions. This analysis also guides future experimental validation work aiming to complete the understanding of the function of RNA modifications in Archaeal translation. Page 1 of 26 (page number not for citation purposes) BMC Genomics 2008, 9:470 http://www.biomedcentral.com/1471-2164/9/470 Background etry techniques [25] (for more recent development of the Post-transcriptional modification of transfer and ribos- technique, see [26] and references therein). However, to omal RNAs is essential for their cellular activities as core date Haloferax volcanii, a Halobacteriaceae that lives opti- molecules of the translation apparatus. To date, the chem- mally at 42°C in the presence of 1.5–2.5 M NaCl [27], is ical structure of more than one hundred RNA modifica- the only Archaea for which both the chemical identities tions have been identified in all domains of life [1-3]. In and positions of almost all modified ribonucleosides have transfer RNAs, modified nucleotides are found predomi- been mapped for nearly the whole set of the 52 sequenced nantly within the 3D-core of molecules and in the antico- tRNAs with distinct anticodons [28,29]. In addition, 13 don arm, especially at the wobble position 34 and at tRNA sequences of two closely related mesophilic halo- position 37, 3' adjacent to the anticodon (conventional philes are available, Halobacterium cutirubrum (12 numbering of tRNA positions is as defined in [4], http:// sequences) and Halococcus morrhuae (one sequence) [4]. www.tRNA.uni-bayreuth.de). These particular modifica- For H. volcanii ribosomal RNAs, the type and position of tions allow the molecules to adopt the canonical L-shaped modifications are available in the case of the 16S RNA conformation and modulate interactions with various [30,31], but not for the 23S nor the 5S RNAs. These can be interacting macromolecules such as aminoacyl:tRNA-syn- inferred from studies on another closely phylogenetically thetases, initiation, elongation and termination factors, related halophilic Archaea Haloarcula marismortui [32,33]. mRNA and/or elements of the decoding and peptidyl- However, while the RNA modifications have been centers of the ribosome (reviewed in [5-10]). In ribos- mapped in RNAs of halophiles, including H. volcanii, the omal RNAs, modified nucleotides are located mostly in identity of the genes that code for the corresponding RNA regions corresponding to the functional centers of the modification enzymes remains largely ignored. ribosome [11-14]. Their location suggests a role in accu- racy and efficiency of translation, however the specific Using a comparative genomic analysis method, that we function of each modified nucleoside is still largely have recently applied to the only other organism with an unknown. This lack of knowledge stems from peculiarities almost complete set of sequenced tRNAs, the pathogenic of the rRNA molecule itself: it is a large molecule (molec- bacteria Mycoplasma capricolum [34], we set out to predict ular mass between 1.5 to 3.9 MDa); some nucleotides are all the RNA modification genes in the halophilic archae- only partially modified and their function(s) are most cer- aon H. volcanii. Some were easily predicted by homology tainly dependent on a network of synergistic interactions with experimentally validated RNA modification genes with different elements of the ribosome, including other from other organisms, while a few are original predictions modified nucleosides that may act cooperatively. Never- based on comparative genomic analysis [35] (not based theless, function has been attributed to modified nucleo- on homology). This computation work provides predic- sides in rRNA in a few cases [13,15-22]. tions that can now guide the experimental validation work with the goals of elucidating the role of RNA modi- Difference in profile and type of RNA modifications fications in Archaeal translation, and ultimately obtaining (Modomics) is one of the criteria that distinguish the a better understanding of the emergence of this extraordi- three kingdoms of life. While universal modifications nary complex enzymatic machinery during evolution. such as Ψ, m5U, t6A or m1G are found in a large numbers of archaeal, bacterial and eukaryal tRNAs, each kingdom Results and Discussion has a set of signature modifications. For examples mimG, Post-transcriptional modification of RNA + 2 6 1 G , m 2Gm, ac A or m Ψ are typical of archaeal tRNAs, Modification pattern of tRNAs while yW, mcm5U and manQ, or k2C, mo5U and m6t6A Thanks to the "tour de force" of Gupta [28,29], a list of are typical of tRNAs from Eukarya or Bacteria respectively almost all of the modified nucleosides present in the dif- (for review see Figure 8.1 in [23]). The same conclusion ferent tRNAs of Haloferax volcanii, a typical mesophilic applies for modified nucleotides in rRNAs (see [24]; http:/ halophile, is available. Figure 1A shows their distribution /people.biochem.umass.edu/fournierlab/snornadb/ (identity and location) in the general 2D-cloverleaf struc- main.php). ture of tRNA, while Figure 1B shows their positions in a schematic 3D-architecture
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  • Isolation and Cultivation of Halophilic Archaea from Solar Salterns Located in Peninsular Coast of India K Asha, D Vinitha, S Kiran, W Manjusha, N Sukumaran, J Selvin

    Isolation and Cultivation of Halophilic Archaea from Solar Salterns Located in Peninsular Coast of India K Asha, D Vinitha, S Kiran, W Manjusha, N Sukumaran, J Selvin

    The Internet Journal of Microbiology ISPUB.COM Volume 1 Number 2 Isolation and Cultivation of Halophilic Archaea from Solar Salterns Located in Peninsular Coast of India K Asha, D Vinitha, S Kiran, W Manjusha, N Sukumaran, J Selvin Citation K Asha, D Vinitha, S Kiran, W Manjusha, N Sukumaran, J Selvin. Isolation and Cultivation of Halophilic Archaea from Solar Salterns Located in Peninsular Coast of India. The Internet Journal of Microbiology. 2004 Volume 1 Number 2. Abstract Two brightly red-pigmented, motile, rod and triangular-shaped, extremely halophilic archaea were isolated from saltern crystallizer ponds located in peninsular coast of India. They grew optimally at salt concentrations between 25 and 35% and did not grow below 20% salts. Thus, these isolates are among the most halophilic organisms known within the domain Bacteria. The isolate HA3 showed optimal growth at 42°C whereas HA9 showed optimal growth at 52°C. These haloversatile microorganisms were presumed as new strains of Haloarcula. H. quadrata (HA3) showed unusual broad spectrum antibiotic resistance pattern. The isolate HA9 was named as H. vallismortis var. cellulolytica due to its peculiar cellulolytic activity, though full taxonomic description is pending. INTRODUCTION 1999; Ventosa et al., 1998). A unique feature of halobacteria Though the oceans are invariably considered as largest saline is the purple membrane, specialized regions of the cell body, hypersaline environments are, particularly, those membrane that contain a two-dimensional crystalline lattice containing salt concentrations in excess of seawater (3.5% of a chromoprotein, bacteriorhodopsin. Bacteriorhodopsin total dissolved salts). Many hypersaline bodies derive from contains a protein moiety (bacteriorhodopsin) and a the evaporation of seawater and are called thalassic covalently bound chromophore (retinal) and acts as a light- (DasSharma and Arora, 2001).