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. 2012:7:11-34.

Decoding in Candidatus Riesia pediculicola, close to a minimal tRNA modification set?

Valérie de Crécy-Lagard  1 , Christian Marck, Henri Grosjean
Affiliations

Decoding in Candidatus Riesia pediculicola, close to a minimal tRNA modification set?

Valérie de Crécy-Lagard et al. Trends Cell Mol Biol. 2012.

Abstract

A comparative genomic analysis of the recently sequenced human body louse unicellular endosymbiont Candidatus Riesia pediculicola with a reduced genome (582 Kb), revealed that it is the only known organism that might have lost all post-transcriptional base and ribose modifications of the tRNA body, retaining only modifications of the anticodon-stem-loop essential for mRNA decoding. Such a minimal tRNA modification set was not observed in other insect symbionts or in parasitic unicellular bacteria, such as Mycoplasma genitalium (580 Kb), that have also evolved by considerably reducing their genomes. This could be an example of a minimal tRNA modification set required for life, a question that has been at the center of the field for many years, especially for understanding the emergence and evolution of the genetic code.

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Figures

Figure 1
Figure 1. Codon/anticodon/tDNA usage for the 20 canonical amino acids in the 14 symbiont genomes and E. coli
The 15 genomes investigated are listed at the top. Full names are given in Supplementary Table SS1. Codon usage within each amino acid family decoding boxes is denoted by the letters on the left: “M” corresponds to most frequently used codon and “m” to the least used ones, with “M1” > “M2” > “m1” > “m2”, etc … to indicate decreasing frequency of codon usage. Rightwards arrows indicate a similar codon usage frequency among the 15 genomes. Details about codon usage in each of the 15 bacteria analyzed can be found in Supplemental Table SS2. These were obtained from automatic determination of all non-overlapping ORFs of 100 codons or more. Vertical bars at the left indicate the six codons of Leu, Ser and Arg respectively. The four columns in the center list the amino acids (indicated as “AA”, one- and three-letter code), the codon (“C”) and anticodon (“AC”) at DNA level. Anticodons never used are indicated as “---”. Numbers at the right indicate the number of tRNA genes harboring the respective anticodons found in each bacteria. Dash signs indicate absence of corresponding tRNA gene. tRNA gene search was performed with tRNAscan-SE [59], and the structure of each tRNA was carefully inspected for fit to the earlier defined bacterial-type tRNA cloverleaf structure [35]. Only three cases of tRNAs (underlined) with more nucleotide than expected (+1 nt in the D-loop) were found. None of the tRNA genes were found in plasmids. The key to the color code is: light gray background denotes four-codon family boxes encoding a single amino acid; yellow background for AUA codon read by the special Ile-tRNA (CAU with wobble C34 modified to k2C34 in mature tRNA, see text); green background for the unique A34-containing tRNAArg (I34 in mature tRNA, see text); red boxes correspond to ‘quartet’ decoding mode in which a single tRNA with T34 at the gene level reads the four codons; blue background denotes C-sparing strategy, the corresponding codon being read by a U34 –containing tRNA. The boxes to the right indicate the standard Genetic Code (split in two).
Figure 2
Figure 2. Prediction of the tRNA modifications present in C. R. pediculicola and comparison with E. coli.
The analysis of the modification genes present in the genome of C. R. pediculicola was performed using the SEED database. We constructed a subsystem containing all known E. coli tRNA modifications genes (see “tRNA modification E. coli” subsystem available on the Public SEED, http://pubseed.theseed.org/SubsysEditor.cgi) and extended it to C. R. pediculicola. A manual search of the genome (NC_014109, NC_013962) using BlastP and tBlastN [60] with the E. coli proteins from the “tRNA modification E. coli” subsystem as input was performed. The gene list used is also found in Table 1 of [61] with the addition of the gene encoding TsaA involved in m6t6A formation (T. Suzuki and V. de Crécy-lagard, personal communication) and TsaD/YgjD involved in t6A formation [16]. In E. coli, IscS and TusABCDE are required for thiol transfer [3], but no TusACDE homologs were found in C. R. pediculicola and SufS is the only IscS homolog in this organism. The m2A37 methylase encoding gene has not been identified in any organism. The same is true for the acp3U47 gene, hence the question marks. We previously predicted yfiF encodes the missing methylase [62], but this has not been experimentally validated. No yfiF homolog or no other methylase of unknown function could be identified in the C. R. pediculicola genome, making the presence of m2A37 in this organism unlikely. Finally, to make sure no other genes had been missed, all known tRNA modification genes from B. subtilis and S. cerevisiae were queried in C. R. pediculicola (using the subsystems “tRNA modification Bacteria”, “tRNA modification yeast cytoplasmic” and “tRNA modification yeast mitochondrial” [63]). The genes present in C. R. pediculicola are listed in the dashed boxes, with prediction of the resulting modification. Assuming that gene products in C. R. pediculicola exhibit the same specificity as the E. coli homologs, one can predict which modifications are found in the 33 tRNAs of the symbiont. They are all localized in the anticodon loop and proximal stem (indicated by numbered grey circles, the whole cluster of modified nucleotides being encircled by dashed line). Only acp3U, normally present at position 47, cannot be excluded because the gene coding for the corresponding enzyme is unknown. For the same reason, it is not certain if m2A37 is present. For comparison, the same tRNA cloverleaf is shown with all the modified nucleotides identified so far by sequencing the 37 fully mature E. coli tRNA, as indicated in Figure 1 (only 4 isoacceptor tRNA remain to be sequenced, see Figure 4). The modified nucleotides common to both bacteria are indicated in black, while the ones found only in E. coli are indicated in grey. In brackets, the number of isoacceptor tRNAs containing a given modification is indicated. When this number is low, the identity of the modified tRNA is also indicated using the one letter code for amino acid. Open circles correspond to positions in E. coli tRNAs where no modification has been found. This compilation was adapted from previously published data [2, 3]. Full names for the different acronyms used to define a given modified base can be found in the MODOMICS database [1].
Figure 3
Figure 3. Prediction of tRNA modifications present in insect symbionts
A signature gene was chosen for every modification and the distribution of the genes analyzed in all genomes listed in Figure 1 by adding them to the “tRNA_modification_E._coli” subsystem on the Public SEED server. Only the genes that were found in at least one of the genomes analyzed other than E. coli are shown, with the exception of the ones responsible for m2A37 and acp3U47 modifications that have yet to be identified in E. coli. Grey boxes denote genes present in all genomes analyzed. Black boxes denote genes present in E. coli and in some of the symbiotic genomes. White boxes denote that a specific gene is missing in a specific organism.
Figure 4
Figure 4. Comparative decoding strategies of C. Riesia pediculicola and E. coli.
In the standard genetic code, each decoding box contains information about identity of nucleotides present in the anticodon loop and proximal stem, as illustrated in the decoding box corresponding to codons UAA/UAG (labeled in figure as “Extended anticodon”). Shown are the nucleotides at positions 32, the three anticodon bases (34–36) and nucleotide-37 (both in grey background) and the sequence of nucleotide 38–40. On the right side of each decoding box, is listed the information for E. coli isoacceptor tRNAs obtained from the tRNA data banks [2, 3]. On the left side of each decoding box, is listed the information for the homologous C. R. pediculicola (Riesia) isoacceptor tRNAs. The identities of the nucleotides were obtained directly from the tRNA gene analysis (this work, Figure 1), while the presence of modified nucleotides was deduced by combining knowledge from the analysis done in Figure 2 with the known modifications at identical positions in the corresponding E. coli tRNAs. The color code is as in Figure 1. In dark green background, are the only four mature tRNAs in E. coli that have not yet been sequenced, only the sequence of the corresponding genes are known. Differences between the two sets of bacterial isoacceptor species are highlighted by red letters. The exact chemical nature of the hypermodified m1G?37 in E. coli tRNALeu is not known [3], so only the m1G moiety was indicated for the insect symbiont tRNA. Also the presence of m2A37 in C. R. pediculicola is questionable (see Figure 2 legend) and indicated as ?m2A.
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